Ecology of social evolution

Ecology of Social Evolution Judith Korb • Jürgen Heinze Editors Ecology of Social Evolution Prof. Dr. Judith Korb ...

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Ecology of Social Evolution

Judith Korb • Jürgen Heinze Editors

Ecology of Social Evolution

Prof. Dr. Judith Korb Universität Regensburg Lehrstuhl für Biologie 1 93040 Regensburg [email protected] Universität Osnabrück Lehrstuhl für Verhaltenbiologie 49080 Osnabrück [email protected]

ISBN: 978-3-540-75956-0

Prof. Dr. Jürgen Heinze Universität Regensburg Lehrstuhl für Biologie 1 93040 Regensburg [email protected]

e-ISBN: 978-3-540-75957-7

Library of Congress Control Number: 2007938885 © 2008 Springer-Verlag Berlin Heidelberg This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilm or in any other way, and storage in data banks. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permission for use must always be obtained from Springer. Violations are liable to prosecution under the German Copyright Law. The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Cover Design: WMX Design GmbH, Heidelberg, Germany Cover photos by courtesy of Judith Korb and Volker Salewski Printed on acid-free paper 9 8 7 6 5 4 3 2 1 springer.com

Preface

The apparently harmonious functioning of insect societies, the well-ordered coordination of packs of cooperatively hunting carnivores, and the seemingly selfless efforts of helpers in some species of communally breeding birds have long fascinated and puzzled naturalists. How, in a world of Darwinian struggle for life and survival of the fittest, can a behavior persist that obviously does not maximize the direct fitness of the actor but instead benefits others at considerable costs to the actor itself? Since early explanations of cooperation and altruism among animals as “good for the species” have been rejected, a number of attempts have been made to reconcile the existence of such behaviors with evolutionary theory. Among these, W.D. Hamilton’s concept of inclusive fitness (also known as kin selection) is most widely applicable. Hamilton (1964) showed that altruistic behavior that benefits other individuals can be stable in evolution if it is directed towards kin. According to Hamilton’s rule, altruism can spread in a population if the fitness benefits of the altruistic act (b) multiplied by the genetic relatedness (r) of the actor to the recipient are higher than the cost (c) in direct reproduction for the altruist: b×r>c Genetic relatedness is therefore of fundamental importance for the evolution of helper systems and animal societies, such as those of social insects in which individuals forgo their own reproduction to help other individuals reproduce. The peculiar sex determination system of Hymenoptera, haplodiploidy, results in an unusually high relatedness among full-sisters, which on a superficial view seems to explain the widespread occurrence of altruistic worker castes in this taxon (ants, bees, and wasps) on relatedness grounds alone. Relatedness has therefore become one main focus of studies on social evolution in insects. The advent of molecular genetic techniques, allowing an easy estimation of nestmate relatedness, further contributed to the focus on relatedness in explaining social behavior. But Hamilton’s rule consists of two additional parameters, the costs (c) and benefits (b) of the altruistic acts, both hidden in the individuals’ ecology and demography and therefore more difficult to quantify. Although their importance was clearly pointed out already in Hamilton’s original work, social insect studies on such factors have long been overshadowed by studies on the genetic composition of their societies. v

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In contrast, investigations on cooperatively breeding birds and mammals traditionally focused more on ecological factors, which delay offspring dispersal and favor philopatry. The importance of ecological factors is probably more apparent in these animals, as they are generally investigated in the field, while many results on social insects come from laboratory studies. Three hypotheses for the evolution of cooperatively breeding in social mammals or birds have been proposed: (a) the ecological constraints hypothesis, according to which independent breeding is difficult because of the limitation of nesting sites or high dispersal mortality; (b) the lifehistory hypothesis, which states that a species’ life-history characteristics limit opportunities for independent breeding; (c) the benefits of philopatry hypothesis, which stresses the long-term direct benefits of staying at the natal nest, such as inheritance of the natal territory. These hypotheses are not mutually exclusive: while ecological constraints (representing the costs of independent breeding) and philopatric benefits (representing the benefits of staying at home) appear to dictate variation in the behavior among individuals of the same species, interspecific differences in life histories can profoundly influence these costs and benefits between species. During recent years, a large amount of data both on genetic and ecological factors influencing social behavior has accumulated, which provides the opportunity for a comparative analysis of social evolution. In this book, we intended to use information from a large range of social taxa, including vertebrates and invertebrates, (i) to investigate the importance of ecological factors and genetic relatedness for the occurrence of social behavior and (ii) to determine whether there are common patterns that favor social life. It appears the time is particularly ripe for such a synthesis because it has repeatedly been argued that relatedness as a driving factor in social evolution has received undue attention and that kin selection is less important than traditionally assumed. We believe that many of these claims are based on misunderstandings about the term “kin selection,” which is too often equated with relatedness. Showing that variation in relatedness does not have the expected outcome on the degree of social behavior, for example, when individuals do not nepotistically feed those to which they are most closely related, does not mean that kin selection does not apply. If feeding more closely related individuals was more costly than indiscriminately feeding all relatives, kin discrimination would not be selected. Approaches like the ‘new group selection’ (multilevel selection, trait-group selection) theory may make it easier to quantify the importance of those factors, which are currently hidden in the costs-and-benefits terms of Hamilton’s rule. However, in contrast to what is occasionally assumed they do not provide real alternatives to kin selection but instead present a different perspective. Kin selection and new group selection are interconvertible. According to new group selection, the evolution of altruism is not favored if the covariance of traits among individuals within a group is not larger than that between groups. Kinship is the most prominent mechanism to create such a covariance. This book attempts to provide a broad overview of the ecology of social evolution across large parts of the animal kingdom. Chapter 1 provides a theoretical background of social evolution and thus prepares the ground for the investigations of

Preface

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sociality in various model systems, starting with the ‘non-classical’ social insects, social aphids (Chap. 2) and thrips (Chap. 3), and the classical societies of social Hymenoptera (wasps, Chap. 4; bees, Chap. 5; ants, Chap. 6) and termites (Chap. 7). Chapters 8–11 cover social vertebrates: birds (Chap. 8), horses (Chap. 9), African mole-rats (Chap. 10), and primates (Chap. 11). In the final chapter (Chap. 12) we try to provide a synopsis on emerging patterns of factors favoring cooperation and altruism among individuals and we outline future perspectives. Taxa that are not covered in special chapters are included in the final chapter, if possible.

Contents

1 The Evolution and Ecology of Cooperation – History and Concepts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Andy Gardner and Kevin R. Foster 2 The Ecology of Altruism in a Clonal Insect . . . . . . . . . . . . . . . . . . . . . . . Nathan Pike and William A. Foster

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3 The Evolutionary Ecology of Eusociality in Australian Gall Thrips: a ‘Model Clades’ Approach . . . . . . . . . . . . . . . . . . . . . . . . . Thomas W. Chapman, Bernard J. Crespi, and Scott P. Perry

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4 The Ecology and Evolution of Helping in Hover Wasps (Hymenoptera: Stenogastrinae) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Jeremy Field

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5 Why are so Many Bees but so Few Digger Wasps Social? The Effect of Provisioning Mode and Helper Efficiency on the Distribution of Sociality Among the Apoidea . . . . . . . . . . . . . . . Erhard Strohm and Jürgen Liebig 6 Social Plasticity: Ecology, Genetics, and the Structure of Ant Societies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Jürgen Heinze 7 The Ecology of Social Evolution in Termites . . . . . . . . . . . . . . . . . . . . . . Judith Korb 8 Kin-Recognition Mechanisms in Cooperative Breeding Systems: Ecological Causes and Behavioral Consequences of Variation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Jan Komdeur, David S. Richardson, and Ben Hatchwell

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Contents

9 Social Ecology of Horses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195 Konstanze Krueger 10 African Mole-Rats: Eusociality, Relatedness and Ecological Constraints . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 207 M. Justin O’Riain and Chris G. Faulkes 11 Genetic and Ecological Determinants of Primate Social Systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Peter M. Kappeler

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12 The Ecology of Social Life: A Synthesis. . . . . . . . . . . . . . . . . . . . . . . . Judith Korb and Jürgen Heinze

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Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Contributors

Thomas W. Chapman Department of Biology, Memorial University, St. John’s, NF A1B 3X9, Canada, [email protected] Bernard J. Crespi Department of Biosciences and Behavioural Ecology Research Group, Simon Fraser University, Burnaby, BC V5A 1S6, Canada, [email protected] Chris G. Faulkes School of Biological and Chemical Sciences, Queen Mary, University of London, Mile End Road, London E1 4NS, UK, [email protected] Jeremy Field Department of Biology, University College London, UK, [email protected] Kevin R. Foster Center for Systems Biology, Harvard University, Bauer Laboratory, 7 Divinity Avenue, Cambridge, MA 02138, USA William A. Foster Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK, [email protected] Andy Gardner St John’s College, Oxford University, St Giles, Oxford OX1 3JP, UK Institute of Evolutionary Biology, University of Edinburgh, King’s Buildings, West Mains Road, Edinburgh EH9 3JT, UK, [email protected] Ben Hatchwell Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK, [email protected] Jürgen Heinze Department Biology I, University of Regensburg, 93040 Regensburg, Germany [email protected]

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Contributors

Peter M. Kappeler Dept. Sociobiology/Anthropology, University of Göttingen & Dept. Behavioural Ecology & Sociobiology, German Primate Center, Göttingen, Germany, [email protected] Jan Komdeur Animal Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, The Netherlands, [email protected] Judith Korb Department Biology I, University of Regensburg, 93040 Regensburg, Germany, [email protected]. Behavioral Ecology, University of Osnabrueck, D-49080 Osnabrueck, Germany, [email protected] Konstanze Krueger University of Regensburg, Department Biology I, Zoology, Universitätsstraße 31, 93053 Regensburg, Germany, [email protected] Jürgen Liebig School of Life Sciences and Center for Social Dynamics and Complexity, Arizona State University, Tempe, AZ 85287-4501, USA, [email protected] M. Justin O’Riain Zoology Department, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa, [email protected] Scott P. Perry School of Biological Sciences, Flinders University of South Australia, GPO Box 2100, Adelaide, SA 5001, Australia Nathan Pike Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK, [email protected] David S. Richardson Centre for Ecology, Evolution and Conservation, School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK, [email protected] Erhard Strohm Department of Zoology, University of Regensburg, 93040 Regensburg, Germany, [email protected]

Chapter 1

The Evolution and Ecology of Cooperation – History and Concepts Andy Gardner(* ü ) and Kevin R. Foster

Abstract We review the historical development of theory on the evolution and ecology of cooperation. Darwin launched this topic of inquiry with a surprisingly modern discussion of how fitness could be derived from both personal reproduction (direct fitness) and the reproduction of family (indirect fitness), and the anarchist Petr Kropotkin forever wove ecology into sociobiology with his book on Mutual Aid. From there, an eccentric group of protagonists took the helm and developed theories of social evolution with clear (although sometimes implicit) links to ecology. Here we provide a summary of the foundational theory, including Hamilton’s rule, neighbormodulated fitness, inclusive fitness, and levels of selection; discuss the classification and semantics of social behaviors; and give a brief overview of the various mechanisms that have been invoked to explain cooperation. Recently, models have emerged that frame the evolution of cooperation in an explicitly ecological context, including the theories of reproductive skew, cooperation in viscous populations, and the tragedy of the commons. In particular, rates and patterns of dispersal strongly influence fitness, the costs and benefits of sociality, and genetic relatedness in social groups. This is an exciting time for ecological sociobiology and there is a great need for studies that combine careful natural history with social evolutionary theory.

1.1

Introduction: The Historical Puzzle of Cooperation

“If it could be proved that any part of the structure of any one species had been formed for the exclusive good of another species, it would annihilate my theory, for such could not have been produced through natural selection.” Darwin (1859) Charles Darwin clearly recognized the problem that cooperation poses for his theory of evolution by natural selection. Natural selection favors the individuals

Andy Gardner Institute of Evolutionary Biology, University of Edinburgh, King’s Buildings, Edinburgh EH9 3JT, United Kingdom [email protected]

J. Korb and J. Heinze (eds.), Ecology of Social Evolution. © Springer-Verlag Berlin Heidelberg 2008

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who have the greatest personal reproductive success, so it is unclear why an organism should be selected to enhance the fitness of another. How then can cooperation evolve? This question has been central to the development of social evolution theory. As we will see in this chapter, solid theoretical foundations have been laid, and the fundamental processes are now well understood. Indeed, Darwin himself seems to have understood the problem rather well. Later in the chapter of The Origin of Species from which the above quote was taken, Darwin discussed two archetypes of social cooperation: the mutualism between pollinators and his beloved orchids, and the death of the stinging honeybee worker. Plant-pollinator traits had, earlier in his book, been linked to individual benefits for each of the parties involved: “individual flowers which had the largest glands or nectaries, and which excreted most nectar, would oftenest be visited by insects, and would be oftenest crossed; and so in the long-run would gain the upper hand”, and worker altruism was to be explained by benefits to the community, which he linked specifically to family relations: “with social insects, selection has been applied to the family, and not to the individual”. Despite his ignorance of the mechanisms of heredity, Darwin had pre-empted the two major classes of modern explanation for social evolution: (1) direct fitness benefits, or an increase in the actor’s personal reproductive success; and (2) indirect fitness benefits, or an increase in the reproductive success of relatives who share genes in common with the actor. Darwin, then, held a fairly sophisticated understanding of social evolution. He also appreciated the importance of ecology as a central shaping force in natural selection. Darwin did not use the word ecology but frequently made reference to “conditions”, which appears to be similar to modern notion of ecology – the relationship between an organism (or population) and its environment. However, he seems to have given less thought to the intersection of ecology and sociality. For this, one had to wait for the eccentric but rich writings of the anarchist prince Petr Kropotkin who launched the 20th century interest in social evolution with his book: Mutual Aid: A Factor in Evolution (Kropotkin 1902). Kropotkin took an unapologetically positivist and biased view of the natural world, providing a long list of examples of animal and human cooperation in an attempt to counter the prevailing Darwinian view of the “harsh, pitiless struggle for life”. Notably, Kropotkin’s musings were ecologically oriented from the very start. His ideas were inspired by how “the struggle against nature”, for which he often cited the terrible Siberian snowstorms, can be a more powerful force than any struggle among members of the same species. On this basis, he argued that cooperation will often evolve rather than competition. From a theoretical standpoint, Kropotkin’s work is a good deal less sophisticated than Darwin’s, and he seems not to have understood the fundamental principles of natural selection as well as his intellectual predecessor. Nevertheless, Kropotkin’s book was an important antithesis to the contemporary focus on competition, and formed a landmark work that introduced two central principles of social evolution: firstly, that cooperation is abundant in the natural world; and secondly, that ecological conditions are central to its evolutionary success. The spirit of Kropotkin’s book, which combined a distinctly ecological perspective with a somewhat naïve view of the underlying evolutionary processes,

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was carried by Allee (1927, 1951) and Wynne-Edwards (1962) into the mid-20th century. Both authors were impressed by how often individuals appeared to cooperate but, like Kropotkin, were somewhat uncritical in their attempts to explain the evolutionary advantage of such behavior. In particular, they were often too ready to appeal to species or population-level benefits for social traits, in an attempt to give an evolutionary explanation for the phenomena that they described. The error in thinking that traits frequently arise through species-level selection is now one of the famous fallacies of evolutionary biology (Williams 1966; Trivers 1985), and we only provide a quick illustration here. Consider the common occurrence of infanticide in many mammals. One might be tempted to infer that individuals kill their own young in order to keep the population size down so as to prevent overexploitation of the available resources. However, it is also clear that, if this were the case, any individual not committing infanticide would enjoy a greater number of descendants than its peers, and therefore such fitness-promoting behavior would be rapidly selected. In other words, the selection of individuals within a sizeable population will usually be more powerful than any population-level selective effects. Unsurprisingly, it turns out that infanticide is frequently driven by one individual killing the offspring of its neighbors, for its own selfish advantage. As we will see below, the differential success of groups (Price 1970; 1972; Hamilton 1975; Wilson 1975) or species (Williams 1966; Nunney 1999; Rankin et al. 2007) can be important in social evolution. However, arguments based on the existence of these processes must be applied very carefully and without neglecting competition between individuals within each of these units (Williams 1966; Trivers 1985). Not all authors were making this error in reasoning. Many contemporaries of Allee and Wynne-Edwards appear to have had a clearer and more modern view of how cooperation could evolve in a world dominated by individual or even genelevel selection. For example, the polymath H. G. Wells, who is better known for his science fiction than for his science fact, likened the beehive to a single organism, with the sterile workers as its somatic tissue. Together with Julian Huxley, and his son G.P. Wells, he reasoned that: “The instincts of the workers can be kept up to the mark by natural selection. Those fertile females whose genes under worker diet do not develop into workers with proper instincts, will produce inefficient hives; such communities will go under in the struggle for existence, and so the defective genes will be eliminated from the bee germ-plasm.” (Wells et al. 1929) An appreciation of how sophisticated sociality could evolve was also apparent in the writings of a number of other authors during this period. This includes R. A. Fisher who, in the following year (Fisher 1930), appealed to benefits for family members in order to explain why it should benefit a caterpillar that has already been eaten to be both colorful and distasteful. Following Wells et al. (1929), further lucid explanations for the evolution of social insect workers were provided by Sturtevant (1938) and Emerson (1939). Notably, although these authors embraced the group-level arguments used by Allee and Wynne-Edwards, they were careful to restrict attention to family groups. Like Darwin, therefore, they avoided the species or group-selection fallacy by correctly combining group and kin

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thinking. Haldane (1932, 1955) similarly explained worker altruism and is more famously remembered for his colorful quip on how many brothers or cousins he would have to trade his own life for in order to, genetically speaking, break even. Haldane (1932) is also notable for sketching a model of ‘tribe-splitting’ that might account for the evolution of altruism, though no concrete results were derived. A comparable group-selection model was later provided by Wright (1945), who pursued the algebra a little further though without producing any concrete results. It is clear, therefore, that several authors understood that social traits can be favoured by natural selection even when they come at a cost to the individual. However, a formal understanding of the underlying processes did not arrive until the 1960s, with Hamilton and the theory of inclusive fitness.

1.2 1.2.1

Hamilton and the Foundations of Social Evolution Theory The Genetical Theory of Social Behavior

Hamilton’s (1963, 1964, 1970) theory of inclusive fitness was arguably the greatest of the contributions to Darwinism made in the 20th century. It not only provided a lucid and quantitative general account of the evolution of social behaviors but it also led to a deeper understanding of natural selection and the elusive concept of Darwinian fitness. It is remarkable that such work emerged at a time when the genetics of behavior was still a highly controversial topic, strongly tied to the recent memory of the eugenics movement. Even more remarkable is that this great contribution to evolutionary theory was the work of a solitary postgraduate student. The young Hamilton’s clear intellectual predecessor was R. A. Fisher, whose masterpiece The Genetical Theory of Natural Selection (Fisher 1930) had placed Darwinism on the firm theoretical foundations of Mendelian genetics. Fisher recast Darwinian fitness as an individual’s genetic contribution to future generation, and described natural selection in terms of changes in gene frequencies. His central result, the fundamental theorem of natural selection, is a mathematical proof of Darwin’s verbal argument that those adaptive traits that are retained by the sieve of natural selection are those that operate to enhance the fitness of the individual (Grafen 2003). A gene causing a behavior that increases the fitness of its bearer will, by definition, be favored by natural selection, and hence those behaviors that accumulate in natural populations will be those that best serve the selfish interests of the individual. Fisher’s proof came with a tantalizing caveat. He explicitly neglected the possibility of interactions between genetic relatives, which he understood could lead to indirect fitness consequences of carrying genes. This means that carrying a particular gene could be associated with having higher fitness, even if the direct effect of the gene was to reduce the fitness of its bearer. This was a nuisance for Fisher, but he did not linger on the problem for too long, suggesting that these would generally

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be unimportant and hence could reasonably be neglected. The naturalist Hamilton, however, saw social interaction between relatives everywhere in nature, and understood the potential for an evolutionary theory of altruism. He set about re-examining the fundamental theory of natural selection in the light of relatedness and the possibility that an individual’s fitness is determined, in part, by the behaviors of its neighbors.

1.2.2

Classification of Social Behaviors

The first step was to provide a formal classification of social behaviors, and Hamilton’s (1964) scheme does this on the basis of the fitness consequences of the behavior for the actor and for the recipient (Table 1.1). Mutually beneficial (+/+) behaviors increase the fitness of the actor and the recipient; selfish (+/−) behaviors increase the fitness of the actor and decrease the fitness of the recipient; altruistic (−/+) behaviors decrease the fitness of the actor and increase the fitness of the recipient; and spiteful (−/−) behaviors decrease the fitness of the actor and recipient (Hamilton 1964, 1970; West et al. 2007a). Typically, cooperation is used to refer to any behavior that increases the fitness of the recipient, i.e., either mutual-benefit (+/+) or altruism (−/+), which have also been grouped together as ‘helping’ behaviors (West et al. 2007a). Of the two ‘harming’ behaviors, selfishness (+/−) poses no conceptual difficulties, as it directly beneficial for the actor. Spiteful (−/−) behavior (Hamilton 1970) is more mysterious and rather neglected by social evolution theory (reviewed by Foster et al. 2001; Gardner and West 2004a); though it has been implicated in microbial and animal conflicts (Hurst 1991; Foster et al. 2001; Gardner and West 2004a; Gardner et al. 2004, 2007a). This classification has not always been followed, and misuse of the terminology has generated much semantic confusion (reviewed by Lehmann and Keller 2006; West et al. 2007a). In particular, it is important to emphasize that this conventional classification is based on total lifetime fitness effects, and not simply the immediate consequences for fecundity or survival. Depending on the ecological context in which the individuals find themselves, there may be a rather complicated link between social behavior and the total fitness effects. This means that it can be far from trivial to determine whether a behavior is beneficial or deleterious for the actor or for any recipients. Furthermore, these fitness effects are absolute (or relative to the population as a whole) and not measured, for example, relative to an individual’s

Table 1.1 A classification of social behaviors, based upon Hamilton (1964, 1970) and West et al. (2007a) Fitness impact for recipient + − Fitness impact for actor

+ −

Mutual benefit Altruism

Selfishness Spite

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immediate social partners. This is important because some researchers later defined altruism in terms of involving a within-group fitness disadvantage (e.g., Wilson 1990), and so including even those behaviors that increase the absolute fitness of the actor when its share of the group benefit outweighs the within-group disadvantage (reviewed by West et al. 2007a; Foster 2008).

1.2.3

Neighbor-Modulated Fitness

If an individual’s behavior can impact the fitness of other individuals, then an individual’s personal fitness can depend upon the behaviors of others. Hamilton (1963, 1964) made explicit the possibilities for an individual’s fitness to be a function of not only its own behavior (and hence the genes underlying this) but also the behaviors of its social partners (and hence the genes present in its social environment), and he termed this ‘neighbor-modulated’ fitness. This neatly partitions the individual’s personal fitness into two components: (1) direct fitness, due to the behavior of the individual itself; and (2) indirect fitness, due to the behavior of social partners (Hamilton 1964; Brown and Brown 1981; West et al. 2007a, 2007b; Fig. 1.1a). Hamilton (1963, 1964) then took a ‘gene’s-eye’ view, and showed that a gene for cooperation (or indeed any behavior) can be favored by natural selection if it

Fig. 1.1 Alternative approaches to fitness. a Neighbor-modulated fitness is the total reproductive success of a focal individual, and is the impact of its own behavior (solid black arrows) on its personal reproductive success (direct fitness) plus the impact of the behaviors of its social partners (solid grey arrows) on its personal reproductive success (indirect fitness). b Inclusive fitness describes the impact of the focal individual’s behavior (solid black arrows) on its own reproductive success (direct fitness) and also the impact of its behavior (solid black arrows) on the reproductive success of its social partners (indirect fitness), the latter being weighted according to the relatedness (broken arrow) of the recipient to the focal individual. This describes how well the individual transmits copies of its genes to future generations, both directly and also via the reproduction of relatives. Because the focal individual is in control of its inclusive fitness, this provides the proper definition of Darwinian fitness in a social context: individuals should behave as if trying to maximize their inclusive fitness

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provides a sufficient direct or indirect fitness benefit for its bearers. This provided a general explanation for the evolution of cooperative behaviors. For example, altruists can be favored by selection provided that they socialize with other altruists. The loss of personal fitness through the direct effect of their genes (manifesting in their own altruism) can be compensated by an indirect effect of copies of those same genes (manifesting in the altruistic behavior of neighbors). By highlighting the importance of indirect fitness effects, Hamilton had effectively rendered Fisher’s fundamental theorem (which neglected these) obsolete. Furthermore, he had shown that the Darwinian notion of individual organisms as agents striving to maximize their personal fitness was naïve. While many of today’s researchers would relish the opportunity to topple such intellectual giants as Fisher and Darwin, Hamilton preferred synthesis over sensationalism, and was deeply concerned by these far-reaching consequences of his theory. Individual organisms do appear to behave as if they have an agenda, and Hamilton was motivated to find out if his formalism could explain precisely what the agenda is (Hamilton 1996). Certainly organisms do not act to maximize their direct fitness, as the evolution of altruism demonstrates. Nor can they be maximizing their neighbor-modulated fitness, because the indirect component of fitness is not under their command but is instead controlled by their social partners.

1.2.4

Inclusive Fitness

Hamilton’s (1963, 1964, 1970) conceptual breakthrough was to break the link between parents and their offspring, and to reassign increments of reproductive success to individuals on the basis of behavior (Fig. 1.1b). This puts the focal individual (the actor) and its behavior firmly in the center of a new fitness accounting scheme (Grafen 1984, 2006). The actor’s direct fitness, being the component of its personal fitness that it can ascribe to its own behavior, remains the same as in the neighbor-modulated fitness view. However, its indirect fitness is now made up of all the offspring of neighbors that can be attributed to its own behavior. A complication is that all non-descendant offspring are not valued equally, and in particular will not usually be as valuable as the actor’s own progeny. For this fitness-accounting scheme to work, and be equivalent to neighbor-modulated fitness, the correct measure of value is provided by the coefficient of relatedness. The actor accrues more indirect fitness from helping a genetically similar relative than it does by providing the same benefit for a less-related neighbor. With relatedness providing an exchange rate (Frank 1998) that allows non-descendant offspring to be translated into effective numbers of descendant offspring, an individual’s direct and indirect components of fitness can be added together to give a total which Hamilton termed ‘inclusive fitness’ (Hamilton 1963, 1964, Brown and Brown 1981). An important point to emphasize, which has resulted in some confusion, is that this logic rests on the change in inclusive fitness affected by the individual’s behavior: the decrease in their own offspring weighted against the increase in relatives’ offspring caused

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by helping. Attempts to evaluate inclusive fitness by counting all the offspring produced in a population that have some positive relatedness to an actor can quickly lead to absurdities (reviewed by Grafen 1982). Natural selection can be viewed as maximizing neighbor-modulated fitness. Equivalently, it can be viewed as maximizing inclusive fitness. These two quantities are simply the fitness measures that emerge from alternative but equivalent accounting schemes for reproductive success (Frank 1998). Both correctly describe the individual’s success in transmitting copies of its genes into future generations, whether this be done directly through its own personal reproductive success irrespective of whose behavior was involved (neighbor-modulated fitness) or else through that reproductive success of its genetic relatives (including itself) which can be attributed to the focal individual’s behavior (inclusive fitness). The benefit of the inclusive fitness view is that it is directly and causally tied to the focal individual’s behavior, and thus better captures the apparent agenda underlying organismal behaviors (Grafen 1984, 2006; Hamilton 1996). Organisms are expected to behave as if they value the reproductive success of their neighbors (devalued according to their genetic relatedness) as well as their own reproductive success. In short, they behave as if they are trying to maximize their inclusive fitness (Grafen 2006). Thus, with inclusive fitness, Hamilton rescued the Darwinian view of natural selection leading to the appearance of agency at the organismal level and showed that Darwinian agents need not be altogether selfish. However, inclusive fitness has often been regarded incorrectly as an altogether separate force in evolutionary biology, which can work against traditional natural selection. Maynard Smith (1964) coined the phrase “kin selection” to describe this apparently new process. This term has stuck despite also giving the impression of a narrowed application of the theory to interactions between kin only. Although close kinship is a robust mechanism for generating genetical relatedness between social partners, inclusive-fitness theory applies more generally to any interactions between genetically similar individuals, irrespective of whether they have a close genealogical relationship (Hamilton 1964a).

1.2.5

Hamilton’s Rule

Hamilton’s theory of indirect fitness effects is encapsulated in the pleasingly simple ‘Hamilton’s rule’, (Hamilton 1963, 1964, 1970), which simply states that a behavior is favored when it leads to a net increase in the inclusive fitness of the actor. −c + br > 0

(2.5.1)

The components of the rule are: (1) the direct fitness cost of the behavior for the actor, c: (2) the fitness benefit for the recipient, b; (3) the genetic relatedness of the recipient to the actor, r. Thus, –c represents the impact of the behavior on the direct fitness of the actor, and br represents the impact of the behavior on the indirect

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fitness of the actor. The rule makes explicit the possibilities for even costly behaviors to be favored, provided they lead to sufficiently large benefits for the actor’s relatives. A derivation of Hamilton’s rule from both neighbor-modulated-fitness and inclusive-fitness perspectives is given in Box 1. Although Hamilton’s rule provides a powerful conceptual aid for reasoning about social evolution, theoretical analyses do not typically use the rule as a starting point. Rather, various different methodologies can be applied to obtain a result that can then be interpreted as a form of Hamilton’s rule, to gain insight into what it means (Taylor and Frank 1996; Frank 1998; Gardner et al. 2007b). One particular methodology that has revolutionized the way in which social evolutionary models are made and analyzed in recent years is the ‘direct’ (neighbor-modulated) fitness approach (Taylor and Frank 1996; Frank 1997, 1998). A sketch of this method is given in Box 2.

Box 1 Derivation of Hamilton’s rule Although Hamilton derived his rule from an inclusive fitness perspective (the effect of the actor on others), it can also be derived from a neighbor-modulated fitness perspective (the effect of others on the actor). The following derivation is due to Queller (1992; see also Frank 1998). We begin by fitting a model of an individual’s fitness (w), as a linear function of that individual’s genetic breeding value (g; Falconer 1981) for a trait of interest and the average genetic breeding value exhibited by its neighbors (g¢), to a population of interacting individuals: w = w + b w ,g i g ′ ( g − g ) + b w ,g ′ i g ( g ′ − g ) + e ,

(B1.1)

where: − w is the average fitness of the individuals in the population; − g is the average genetic breeding value of the individuals in the population; bw,g•g¢ is the least-squares partial regression of the individual’s fitness on its own genetic breeding value; bw,g¢•g is the least-squares partial regression of the individual’s fitness on it’s partners’ average genetic breeding value; and ε is the uncorrelated error. From Price’s (1970) theorem, the change in the average genetic −) is given by: breeding value due to the action of natural selection (∆g w∆g = Cov(w, g ),

(B1.2)

where ‘Cov’ denotes a covariance. Substituting our model into this, we have: w∆g = b w,g i g′ Cov(g, g ) + b w,g′ i g Cov( g ′, g ),

(B1.3) (continued)

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Box 1 (continued) − > 0) so a condition for the average breeding value of the trait to increase (∆g is: b w, g • g ′ + b w, g ′• g

Cov( g ′, g ) > 0. Cov( g, g )

(B1.4)

Note that this is based on the assumption that Cov(g,g), which is the additive genetic variance, is nonzero, and hence is necessarily a positive quantity. This condition for increase is Hamilton’s rule, in its neighbor-modulated fitness guise. The additive effect of the individual’s own genetic breeding value for the trait of interest, holding fixed the effect of its neighbors’ genes, is bw,g•g′ = −c, i.e., it describes the direct cost of the social behavior. Similarly, the effect of the neighbors’ average breeding value on the focal individual’s fitness is the indirect fitness (in the neighbor-modulated sense) benefit bw,g′•g = b. Finally, the ratio of the two covariances can be rewritten as the least-squares regression of an individual’s social partners’ breeding values on its own breeding value (bg′,g), and is equal to the coefficient of relatedness (r; Queller 1992; Frank 1998). Substituting these terms in gives the more familiar Hamilton’s rule: −c + br > 0. We have assumed a population in which all individuals are equivalent. The derivation of Hamilton’s rule in class-structured populations has been given by Taylor (1990). Using this assumption of equivalence, we can readily derive the inclusive fitness version of Hamilton’s rule. Simply, if the effect of genes in one’s social environment (g′) on one’s fitness (w) is bw,g¢•g, then by symmetry this is also equal to the impact of one’s genes (g) on the fitness of neighbors (w¢ ), which can be written as bw¢,g•g¢ (Queller 1992). Substituting into inequality (5), we have: b w, g • g ′ + b w ′ , g • g ′

Cov( g ′, g ) > 0, Cov( g, g )

(B1.5)

which makes explicit the partitioning of the inclusive fitness effect (left hand side of inequality (B1.5) ) into direct and indirect fitness components. Moreover, this emphasizes that the behavioral effects of genes carried in neighbors do not count towards inclusive fitness (the regressions are partial, with respect to g, and holding g′ fixed; Hamilton 1964; Grafen 1984).

1.2.6

Levels of Selection

Although Hamilton’s genetical theory of social evolution was in part developed as an antidote to careless appeals to group or species-level benefits for cooperation (Allee 1951; Wynne-Edwards 1962), recent years have seen renewed interest in the

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Box 2 ‘Direct’ (neighbor-modulated) fitness approach Although inclusive fitness is a conceptually easier way of understanding social behavior (Taylor et al. 2007), and indeed is the proper way of thinking about social adaptations in a Darwinian sense (Grafen 2006), it is often technically simpler to analyze models of social evolution using a neighbor-modulated fitness approach. Here, we outline one popular approach that has been very successful in recent years (Taylor and Frank 1996; Frank 1997, 1998; Taylor et al. 2007; see also Rousset 2004). Confusingly, it has often been termed a ‘direct fitness’ approach, though ‘neighbor-modulated fitness’ is a preferable alternative that does not conflict with prior usage of the terms ‘direct’ and ‘indirect’. The approach is based on the reasonable assumption of vanishing genetic variation in the social evolutionary traits of interest (Taylor and Frank 1996; Frank 1998). We may write fitness (w) as a function of the individual’s genetic breeding value (g), that of its neighbors (g′ ), and the population aver−); i.e., w(g,g′,g −). We assume that fitness is a differentiable function of age (g each of these genetic arguments and, using the chain rule of differential calculus, we can write: dw ∂w ∂w dg ′ = + × . dg ∂g ∂g dg

(B2.1)

Evaluating at g = g′ = − g , due to the assumption of vanishing genetic variation, the partial derivatives can be reinterpreted as the cost and benefit components of Hamilton’s rule, i.e., ∂w/∂g = bw,g•g¢ = −c and ∂w/∂g′/ = bw,g¢•g = b, and the derivative of neighbor breeding value by one’s own breeding value is the coefficient of relatedness dg′/ dg = r (Taylor and Frank 1996; Frank 1998). Setting Eq. (B2.1) to zero, and solving for − g = g*, we obtain an equilibrium point that can then be assessed for evolutionary and convergence stability (Maynard Smith and Price 1973; Eshel and Motro 1981; Taylor 1996). Again, we have assumed for simplicity that all individuals can be treated as if they are equivalent, though class-structure is readily implemented, as described by (Taylor and Frank 1996; Frank 1998; Taylor et al. 2007).

theory of levels of selection (e.g., Keller 1999; Okasha 2006). After the development of the inclusive fitness theory, Hamilton and Wilson pointed out the usefulness of an alternative approach that phrases social evolution in terms of selection between and within groups, rather than separating individual fitness into direct and indirect components (Hamilton 1975; Wilson 1975). However, the theory of group selection has historically been plagued by unfortunate confusion and controversy (above) that has somewhat left it in the wings, as compared to inclusive-fitness theory, which has matured as a field of study, boasting formal though conceptually simple foundations,

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and enjoying very good empirical support. At present, group-selection theory comprises a large amount of verbal discussion and a collection of mathematical models that appear to provide helpful insights but are lacking in conceptual unity (see Okasha 2006 for a recent review). A formal basis for the theory of group selection has been suggested by Hamilton (1975), building upon the work of the tragic genius George Price. Price’s (1970) theorem, which underpins the canonical derivation of Hamilton’s rule (Hamilton 1970), has also been applied to levels of selection in evolution (Price 1972; Hamilton 1975). This approach partitions the total evolutionary response to selection into distinct between-group and within-group components. Importantly, it does this in a completely general and formal way, and so can be applied to any model, providing a common foundation upon which to rest any group-selection analysis. This partition can be very useful for conceptualizing the potential tension between the interests of individuals and the needs of the group (Hamilton 1975). When these interests come into conflict, Price’s approach allows their relative strengths to be compared and the balance between these two evolutionary pressures to be determined in a precise, quantitative way. However, there are some important caveats. It can often be difficult to decide which particular collections of individuals constitute groups, and yet this decision has important consequences for how we ascribe evolutionary change to group selection. Also, the approach can lead to apparent absurdities, such as diagnosing the operation of group selection even when considering non-social traits (Heisler and Damuth 1987). For example, if physical strength enhances individual fitness in a straightforward way, then some groups will be fitter than others simply because they contain, by chance, stronger individuals. The consensus in the group-selection literature seems to be that identifying this as ‘group selection’ is incorrect. An alternative approach, termed ‘contextual analysis’ (Heisler and Damuth 1987), mirrors the neighbor-modulated fitness approach discussed above, and describes individual fitness as a function of its own behavior and also the behavior or other characteristics of its group. A least-squares regression analysis identifies the impact of the group character on individual fitness as a description of ‘group selection’. This procedure avoids the incorrect diagnosis of group selection in the hypothetical example of individual strength. However, it has its own difficulties (Heisler and Damuth 1987; Goodnight et al. 1992). If we consider again the selection for individual strength, but now assume soft selection (Wallace 1968) is in operation so that every group is constrained to have the same total fitness, then an individual with particularly strong group mates will tend to have lower fitness than it would in another group. Contextual-analysis diagnoses group selection in this scenario, because individual fitness depends on the group environment. However, group selection is typically phrased in terms of fitness differences between groups, so there appears to be a mismatch between the formalism and the fundamental process that it was intended to capture. Thus, while a levels-of-selection (or contextualanalysis) perspective can be very useful for describing and conceptualizing social evolution, a fully satisfying formal theory of group selection (defined as the differential success of groups) remains to be developed.

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It is important to emphasize that the levels-of-selection approach does not suppose that a different type of natural selection is in operation, but rather it provides an alternative way of conceptualizing the same process of natural selection that is described by inclusive fitness theory (Hamilton 1975; Grafen 1984). Indeed, both derive from the same fundamental evolutionary theorem (Price 1970, 1972), and it is usually straightforward to switch between these different views when considering a particular model. The contentious ‘levels-of-selection’ debate has long been solved, or rather it has been shown to be empirically vacuous, turning, as it does, upon an issue of differences in approach rather than any real disagreement as to how natural selection operates (Reeve and Keller 1999).

1.3 Mechanisms for the Evolution of Cooperation 1.3.1

General Overview

Hamilton provided a general explanation for the evolution of cooperation, or indeed any social behavior; namely that the behavior is favored if it increases the actor’s inclusive fitness. Thus, explanations for cooperation rely on either direct fitness benefits (i.e., mutual benefit) or else indirect fitness benefits (i.e., altruism) (Brown 1987). Although this says nothing about the actual mechanisms involved, it is helpful to distinguish mechanisms supporting the evolutionary maintenance of cooperation on the basis of direct versus indirect fitness benefits (Fig. 1.2). We emphasize that mechanisms need not be mutually exclusive, and cooperation will often be dependent on a mixture of direct and indirect fitness benefits. The following tour of mechanisms is based upon the recent reviews of Sachs et al. (2004), Lehmann and Keller (2006) and West et al. (2007a, 2007b).

Fig. 1.2 A classification of mechanisms favoring the evolution of cooperation, based upon West et al. (2007a, 2007b)

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1.3.2

Direct Fitness Benefits

1.3.2.1

Non-Enforced

By-product benefits – The simplest explanations for cooperation involve directfitness benefits that arise naturally from the behavior, and where the benefit to other parties can be regarded as a fortunate side effect (Sachs et al. 2004). Such by-product benefits are exemplified in Hamilton’s model of the ‘selfish herd’ (Hamilton 1971). In the simplest form of herding behavior, an individual that joins a herding group will gain a personal benefit from protection against predators. At the same time, however, group fitness is also increased, so there is no individual and group conflict. An interesting possibility is that species-level selection favors cooperative systems with cooperation based upon by-product benefits, or equivalently, species where a group member has intrinsic constraints on the evolution of cheating. For example, it has been suggested that social species that arise with pleiotropic constraints between potential cheating strategies and a personal cost will persist better than those where cheating can readily arise. This predicts that the genome to phenome mapping in extant social species will tend to constrain cheating (Foster et al. 2004, 2007; Rankin et al. 2007). Feedback benefits – A related form of direct fitness benefit comes when an individual’s direct fitness is dependent on the success of other members of its group, or a shared group trait. When this occurs, an actor can be selected to cooperatively invest in the group in order to ensure their own personal prosperity. What makes this arguably distinct from by-product benefits is that, while both increase group fitness, with feedback benefits the action will tend to decrease the relative fitness of the individual in the group. An example of this, which has been termed ‘weak altruism’ in the group-selection literature, is cooperative nest founding by multiple ant queens where all queens will work to ensure the colony’s success because this later feeds back on their reproductive success (Wilson 1990). These feedbacks (along with kinship) are also probably important in vampire bats that share blood with others in their roosting group. By sharing, they ensure the survival of the group and the later receipt of blood when they themselves fail to forage (below, Foster 2004). More generally, such feedback effects are central to the evolution of between-species cooperation (Sachs et al. 2004), where one species invests in another species because its own success is dependent on the success of its mutualist (‘partner-fidelity’ feedback). For example, ants that live symbiotically in a plant will be often selected to invest in the survival, if not always the reproduction, of their host (Yu and Pierce 1998; Foster and Wenseleers 2006).

1.3.2.2

Enforced

Cooperation can also be enforced. That is, cooperation by an actor is often encouraged by specific adaptations in its social environment that function to make

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defection costly. It is important in discussing enforcement to recognize that there are two levels. There is what might be called ‘primary enforcement’, where cooperation is promoted in an actor with the facultative return of cooperation by the recipient and then there is ‘secondary enforcement’, which involves a separate currency or currencies of punishment or reward, such as actively harming a defecting individual. Secondary mechanisms, however, carry additional costs to the enforcer, and only seem likely when first-order enforcement is not possible. That is, secondary enforcement is only expected if a potential enforcer is either noncooperative, or their cooperation is not directed specifically at the defecting individual. For example, most cooperation by social insect workers is directed at the colony as a whole, through behaviors like guarding, brood rearing, and nest building (Wilson 1971), which limits their ability to engage in primary enforcement by redirecting their cooperation away from a particularly rebellious worker. Primary enforcement – Primary enforcement can be viewed from two equivalent perspectives: as rewarding cooperation with cooperation, or punishing defection with defection. Trivers (1971) showed that such conditional behavior will readily promote cooperation in a world where individuals can recognize and remember others. He termed this ‘reciprocal altruism’, but it is better described as ‘reciprocal cooperation’ because it derives a direct fitness benefit and is thus mutually beneficial rather than altruistic (West et al. 2007a). This idea was later developed in the ingenious computational tournaments of Axelrod and Hamilton (1981) who presented programmers with a challenge: in a game of repeated interactions where cooperation leads to mutual gain, but exploitation of other cooperators leads to even greater gain (the ‘Prisoner’s dilemma’), design a winning behavioral strategy. Despite the submission of some complex programs, the winning strategy was very simple: “Tit for Tat” (TFT). This strategy would cooperate in the first round, and subsequently mirror the play of its partner from the previous round. It is reciprocal cooperation, as when TFT encounters a cooperator they enjoy a cooperative interaction, but TFT will not allow its cooperation to be exploited by a defecting partner. Following Axelrod and Hamilton (1981), many theorists picked up on the Prisoner’s dilemma game, often more as a mathematical problem than a biological one, and now there are a myriad of variants on both the scenario and its solution (reviewed by Doebeli and Hauert 2005; Lehmann and Keller 2006). A closely related idea is that of indirect reciprocity, whereby helping others improves one’s reputation, which then increases the chances of being helped (Nowak and Sigmund 1998; Mohtashemi and Mui 2003; Panchanathan and Boyd 2004; Semmann et al. 2004). Along with reciprocal cooperation, indirect reciprocity appears to be very important in human cooperation, but the requirement for recognition and memory of others means they probably occur in relatively few other species (Hammerstein 2003). More generally there are many active behavioral mechanisms that reward cooperative behavior in social interactions, but do not require the recognition and memory of reciprocal cooperation. Central to this is the idea of partner choice, where individuals either preferentially interact and/or cooperate with the more cooperative individuals in a population (Bull and Rice 1991; Noe and Hammerstein

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1994; Ferriere et al. 2002; Johnstone and Bshary 2002; West et al. 2002a; Sachs et al. 2004; Foster and Wenseleers 2006). Theory suggests that partner choice is central to the evolution of between-species cooperation because, being behavioral, it is both local and rapid in effect (West et al. 2002b; Foster and Kokko 2006; Foster and Wenseleers 2006). In support of this, a large body of empirical data is emerging that suggests that partner-choice mechanisms are widespread and common in many mutualisms (Sachs et al. 2004; Foster and Wenseleers 2006). A familiar example of this is the ability of pollinators to rapidly leave plants that do not provide them with enough nectar, which means that pollinators tend to carry the pollen of cooperative plants rather than those that cheat the mutualism (Darwin 1859; Smithson and Gigord 2003). Another example, which is often discussed in terms of punishing sanctions, is legumous plants that appear to shut off the oxygen supply to root nodules inhabited by rhizobial bacteria that have not contributed enough fixed nitrogen to their host (West et al. 2002a, 2002b; Kiers et al. 2003; Simms et al. 2006). Secondary enforcement – In many social species, including humans, systems of enforcement occur that are separate from primary cooperation (Oliver 1980). This raises the problem of why reward or punish cooperation, given that it can be costly to do so (Sober and Wilson 1998; Fehr and Gachter 2000; Sigmund et al. 2001; Boyd et al. 2003)? Like primary cooperation, this can again be answered by direct or indirect fitness benefits (Gardner and West 2004b). An important corollary is that although rewarding behaviors can favor cooperation, by doing so they automatically generate the need for continued rewards. In contrast, punishment can favor cooperation, and once it is established, there is no further need to punish. Thus, systems of rewards are inherently costly and systems of punishment, cheap (Gardner and West 2004b), which may explain the apparent prevalence of punishment and the rarity of rewarding in the natural world (Clutton-Brock and Parker 1995). Another type of negative secondary enforcement, which may be termed policing (Starr 1984; Ratnieks 1988; Frank 1995), operates when the system is organized so that the individual simply cannot gain through uncooperative behavior. When there is no avenue for cheaters to gain an advantage within their group, individuals can only enhance their own fitness by cooperatively improving the fitness of the group as a whole (Frank 2003; Wenseleers et al. 2004a; Ratnieks et al. 2006; Wenseleers and Ratnieks 2006a, 2006b). For example, within honeybee colonies, unmated workers can lay unfertilized eggs that would develop into males that compete with the queen’s sons if left to develop. But workers are selected to destroy each other’s eggs (worker policing), because they are more related to the sons of the queen (their brothers) than they are to the sons of other workers (their nephews; Starr 1984; Ratnieks 1988). Although worker egg laying does occur, it is much rarer than is predicted by theory in the absence of policing (Wenseleers et al. 2004a; Ratnieks et al. 2006; Wenseleers and Ratnieks 2006b). Striking empirical support for this comes from a comparison with colonies in which the queen has died, where policing breaks down. Under these conditions, many workers develop their ovaries and compete over reproduction (Wenseleers and Ratnieks 2006b).

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As with the origin of primary cooperation (by-product benefits, above), any enforcement system will only be evolutionarily stable if they evolve in a way that cannot be evaded. This again, therefore, predicts that trade-offs or pleiotropic relationships will be important, and that the enforcer will exploit them to prevent evasion by an enforcee. A nice example of this is the cooperative bioluminescence caused by the bacterium Vibrio fischeri bacterial symbionts that live in the lightemitting organ of the bobtail squid Euprymna scolopes. The symbiotic relationship is based upon the bacteria providing bioluminescence that might aid the squid in darkness or camouflage it from below against the bright ocean surface. Amazingly, the squid appears able to enforce light production in the bacteria by creating an environment in which the gene for light production is also pleiotropically required for bacterial growth (Visick et al. 2000; Sachs et al. 2004; Foster et al. 2007).

1.3.3

Indirect Fitness Benefits

1.3.3.1

Limited Dispersal

Probably the most widely applicable mechanism for generating indirect fitness benefits for cooperation is population viscosity, or limited dispersal, leading to genetic structuring of populations (Wright 1945; Hamilton 1964, 1971). This means that even indiscriminate altruistic behavior incurring a personal cost and providing a benefit to neighboring individuals could enhance the actor’s inclusive fitness because those neighbors are on average closely related kin (Hamilton 1964, 1971). This promises to be a very general explanation, because it requires no complicated cognitive faculty that allows the discrimination of kin and ensuing nepotism, and thus applies to simple organisms such as bacteria. For example, siderophores are compounds exuded by bacteria to promote iron-uptake (Guerinot 1994; Ratledge and Dover 2000). These compounds are costly for the individual to produce but can be used by any cell in the vicinity, and so may represent an altruistic public good (West and Buckling 2003). Selection experiments that impose a low-dispersal, viscous population structure can result in an evolutionary response for the bacteria to increase their average production of siderophores, due to the increased indirect fitness benefits accrued through the neighboring cells being closely related kin (Griffin et al. 2004). However, things are not so straightforward. As well as generating high relatedness between neighboring individuals, population viscosity can also lead to intensified competition between relatives, which can inhibit the evolution of cooperation (see section 1.4.1).

1.3.3.2

Kin Discrimination

Increased relatedness to the recipients of one’s cooperation (and hence an increased indirect fitness benefit) can be achieved if individuals have the ability to recognize their kin and to bias their cooperative behavior towards them. Kinship can be inferred on the basis of ‘environmental’ cues (Grafen 1990), such as close proximity

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in the natal nest, and the retention of this memory and its influence on social behavior later in life. For example, environmental cues are central to the evolution of the impressive cooperation in social insects, where kinship is typically indirectly inferred from cuticular chemicals that are acquired through presence in the nest (Singer 1998). In addition, kinship is inferred by song similarity in some cooperatively breeding birds (Hatchwell et al. 2001) Alternatively, kinship could be inferred on the basis of genetically determined phenotype and hence shared genes (Grafen 1990). If the main cause of genetic similarity is genealogical closeness, then a social partner who shares one or several ‘marker’ genes in common with the actor will likely share many genes in common, including those encoding cooperation, through recent co-ancestry. For example, sterile ‘soldier’ larvae among the polyembryonic parasitoid wasp Copidosoma floridanum discriminate and protect their closest kin on the basis of the composition of their extraembryonic membrane yet aggressively attack other individuals sharing the same internal environment of the host (Giron and Strand 2004). However, genetic kin recognition is relatively rare, perhaps due to the difficulty of maintaining genetic variability at the marker loci (Crozier 1986; Rousset and Roze 2007).

1.3.3.3

Greenbeards

To demonstrate that it is genetical relatedness rather than genealogical relationship that forms the fundamental basis of indirect fitness benefits, Hamilton (1964) outlined an interesting thought experiment. Supposing that the bearer of a cooperative gene could directly recognize and preferentially aid other carriers of that gene, then cooperation would be favored by natural selection even if these individuals were not genetically similar at any other loci. This could happen if the gene for cooperation also had a pleiotropic effect, which advertised that its bearer was a carrier of the gene. Alternatively, the cooperation, advertisement and recognition functions could be encoded by separate but closely linked genes that would segregate as a single Mendelian unit, i.e., a supergene. Dawkins elaborated on this idea in his book The Selfish Gene (Dawkins 1976), in a memorable illustration in which the advertisement for possession of the gene was the growth of a conspicuous green beard. Such ‘greenbeard’ altruism has been implicated in the stalk-forming behavior of social amoebae. Here, a cell-adhesion protein encoded by the csaA gene is responsible for both the commitment to altruistic stalk-formation and also for gaining access to the social group in the first place (Queller et al. 2003). Interestingly, Hamilton’s thought experiment also permitted a darker interpretation in which a greenbeard gene that caused harm towards neighbors not bearing the conspicuous marker could also be favored (Hamilton 1964), and this could explain even downright spiteful behaviors (Gardner and West 2004a). Such a mechanism has been discovered in the fire ant Solenopsis invicta, where workers carrying a variant of the gp9 gene kill non-carrier queens in multiple-queen colonies (Keller and Ross 1998, Foster et al. 2001; Krieger and Ross 2002). Although greenbeard genes are superficially similar to kin discrimination, and both are based upon genetic relatedness, the details of the inference of genetic

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similarity are quite different. Kin discrimination relies on the inference of genealogical closeness and hence a high expected genetic similarity over all loci, including the cooperation loci, whereas the greenbeard mechanism relies on the inference of genetic similarity at the cooperation loci due to pleiotropy or physical linkage. However, in practice, elements of both kinship and greenbeard recognition will usually be involved when genetic markers are used to infer relatedness as cooperation loci (West et al. 2007b) It is important to emphasize that the greenbeard theory was not intended to represent a plausible mechanism for the evolution of cooperation, but rather it provided an illustration that highlighted that genetic similarity and not genealogical closeness per se is the basis of genetic relatedness. In principle, the greenbeard mechanism does provide an explanation for cooperation, but in practice there are several reasons for suspecting it to have only a minor role to play. In particular, if a new allele were to arise by mutation at the greenbeard locus that could encode the beard (and thus enjoy receiving cooperation) without committing itself to cooperation, then this would be strongly favored by selection (Roberts and Sherratt 2002). Also, a greenbeard gene that produces relatedness only at a single locus will generate conflicts with the rest of the genome that does not share the same relatedness patterns across individuals. As a result, there is expected to be strong selection for modifier genes elsewhere in the genome that disrupt the expression of this costly cooperation (Okasha 2002; Grafen 2006; Lehmann and Keller 2006; Helantera and Bargum 2007). Thus, greenbeards that arise in the absence of associated whole-genome relatedness are expected to typically have a transient existence over evolutionary timescales.

1.4

Making the Ecology Explicit

The general overview of the previous section has focused on the act of cooperation, and has provided a sketch of physical and behavioral mechanisms that can make cooperation mutually beneficial, as well as behavioral and genetic mechanisms that ensure sufficient relatedness between actor and recipient for even altruistic cooperation to be favored. The ecology of social organisms has been largely implicit. However, an understanding of the population and its environment is critical as ecology impacts on every component of inclusive fitness. Within Hamilton’s rule, the direct cost (c) and benefit (b) of a social behavior are meaningless except within the context of a population of individuals competing for genetic representation among future generations, and the genetic structure of social groups, which determines the coefficient of relatedness (r), is crucially dependent upon population processes. Furthermore, in recent years, some areas of theoretical sociobiology have started to more explicitly consider ecology and its effects of social evolution. Here we briefly review three such areas: (1) the theory of reproductive skew, (2) cooperation in viscous populations, and (3) the tragedy of the commons.

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Ecological Constraints and Skew Theory

One of the most fundamental behavioral decisions that social organisms make is whether to remain in their group or, conversely, to leave the group and go it alone (Stacey and Ligon 1991). Not all social organisms have this option (workers in many social insects are unable to mate or found a new colony) but there are many where dispersal decisions shape the social group. This includes many of the lessderived social insects (Bourke and Franks 1995; Queller and Strassmann 1998; Ratnieks et al. 2006) but also many groups of charismatic social vertebrates (Emlen 1991; Hatchwell and Komdeur 2000; Clutton-Brock 2002; Griffin and West 2003), which have helper individuals that remain in the social group and aid in the care of their relatives’ offspring. The study of these groups has consequently focused on the costs and benefits of dispersal, and understandably central to this is the notion of ecological constraints (Keller and Reeve 1994; Emlen 1995; Pen and Weissing 2000; Kokko et al. 2001; Lehmann et al. 2006). If dispersal and group founding is costly and risky, it will often pay, in a fitness sense, to stay and help in an established group, even if the individuals that you raise are less related to you than your own offspring. This logic has been much discussed in the vertebrate literature where, in addition to ecological constraints from dispersal, there may also be explicit benefits for remaining in the group, such as when this group occupies a particularly good territory (Stacey and Ligon 1991) or when large groups have higher fitness than small ones (Kokko et al. 2001). Similar ideas underlie the theories of “reproductive-head start” (Queller 1989) and “assured-fitness returns” (Gadagkar 1990) for the evolution of sociality in insects, which both emphasize that nests take time and are risky to found, so staying with an established nest can have strong fitness advantages. The most theoretical attention to these ecological costs and benefits, however, came through the rapid but ephemeral rise of skew theory in the 1990s, which sought to explain patterns of reproductive sharing among individuals in animal societies. That is, why is it that in some social species many individuals reproduce (low skew) while in others it is restricted to one or a few individuals (high skew)? Skew theory started with a simple expansion of Hamilton’s rule by Vehrencamp (1983a, 1983b), who modeled a social group containing two individuals: a subordinate, who can choose to stay or leave; and a controlling all-powerful dominant, who can choose to cede some reproductive rights to the subordinate. After Vehrencamp, things went quiet for a decade or so, but they were resurrected and extended by Reeve and Ratnieks (1993) and Keller and Reeve (1994). Predictions from skew theories rest upon two key ecological factors: (1) the expected personal success of an individual who leaves the colony and attempts to found a new group on their own (x, dependent upon ecological constraints); and (2) the benefit to the original colony if the individual stays and helps (k – 1, where k is the group productivity with the subordinate, and 1 is without). From Hamilton’s rule, this predicts that a subordinate will be favored to disperse from the social group when:

1 The Evolution and Ecology of Cooperation – History and Concepts

x > r (k − 1),

21

(4.1.1)

where r is genetic relatedness between subordinate and dominant. However, when the subordinate can be very helpful to the dominant, it will pay the dominant to give some reproduction to the subordinate and attempt to make them stay. This staying incentive (s), representing the proportion of group reproduction given over to the subordinate) will select for the subordinate to stay when: x < sk + r[ k (1 − s ) − 1],

(4.1.2)

and one can calculate a similar equation for peace incentives that reduce fighting in the social group (Reeve and Ratnieks 1993; Keller and Reeve 1994). From this simple beginning, skew theory rapidly diversified into a comedy of additional models, each differing in their specific assumptions on the relative power of the individuals, the information available, and whether and how the individuals negotiate their reproductive share (e.g., Reeve et al. 1998; Robertson et al. 1998; Cant and Johnstone 1999; Johnstone and Cant 1999a, 1999b; Johnstone et al. 1999; Kokko and Johnstone 1999; Ragsdale 1999; Cant and Johnstone 2000; Crespi and Ragsdale 2000; Hamilton 2000; Johnstone 2000; Reeve 2000; Reeve and Emlen 2000; Nonacs 2001, 2002; Jeon and Choe 2003; Reeve and Jeanne 2003). What became rapidly evident is that the relationship between the key variables like skew, group productivity, relatedness, and ecological constraints are extremely labile and differ greatly depending on which assumptions are used. One could therefore always find some support for the theories no matter what was found empirically (Reeve and Keller 2001; Heg et al. 2006; Nonacs 2006; Nonacs et al. 2006). While the emphasis on ecology seen in skew models is commendable, their inability to make clear predictions has been a big problem. A possible solution is to focus instead on testing the different models’ assumptions. However, assessing key assumptions such as whether a dominant actually concedes power rather than has it taken from them is not trivial (Clutton-Brock 1998), and the number of assumptions required to make predictions rises rapidly when more than two individuals interact (Johnstone et al. 1999). Further troubles for skew models come from the fact that some easily lose evolutionary stability (Kokko 2003), and that the fitness advantages given by the common assumption of sophisticated decision-making behavior can be very small relative to much simpler behavioral strategies that seem much more realistic (Nonacs 2006). In summary, skew theory provides general support for the importance of ecology in social evolution but, arguably, has not succeeded in incorporating ecology into social evolution theory in a more meaningful way than is achieved by Hamilton’s original work. This is made particularly evident by the rise of the simpler “tug-of-war” skew models (Reeve et al. 1998; Reeve 2000; Langer et al. 2004; Heg et al. 2006), which assume that no individual has complete control, and whose principle prediction mirrors that of Hamilton’s rule : that decreased relatedness will decrease group performance.

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1.4.2

A. Gardner, K.R. Foster

Cooperation in Viscous Populations

One of the earliest attempts to give a quantitative account of the evolution of cooperation was that of Wright (1945) who, in a book review article, outlined the argument that altruism could be favored in the context of viscous population structure. Wright framed this argument in terms of group selection, and was able to provide an approximation for the ratio of the variance between and within groups under varying degrees of dispersal. He understood that individual dispersal would diminish this genetic structuring of the population, and hence slow the action of within-group selection against altruists, but also that some dispersal is required to spread this altruism over the whole population. From this, Wright reasoned that altruism would be most favored with a tiny but nonzero rate of dispersal. However, a mathematical proof for this was lacking. Hamilton (1964a, 1971) picked up the thread in his account of inclusive fitness, and reframed Wright’s scenario in terms of population viscosity leading to a high coefficient of relatedness between actor and recipient. Setting the argument in more explicitly ecological terms, Hamilton (1964, 1971, 1975) revealed the previously hidden problem of kin competition, and drew attention to an earlier treatment by Haldane (1923) who had shown that this could reduce the between-family differences in fitness that are crucial in this context. Limited dispersal not only brings relatives together to socialize, but also to compete for resources, and this could work to inhibit the evolution of cooperation. Having outlined this important caveat, Hamilton nevertheless argued that viscous populations would be those in which we would most expect to see altruism flourishing. Much later, Wilson and colleagues (Wilson et al. 1992) performed simulations of cooperation evolution in purely viscous populations of the sort discussed by Wright to provide a more accurate quantification of the limited dispersal effect. Surprisingly, they could find no appreciable impact of the rate of dispersal on the evolution of cooperation. This puzzling simulation study was soon followed by an analytical ‘island’ model by Taylor (1992a), who used an inclusive fitness approach to recover the same result. Amazingly, whether asexual or sexual reproduction was assumed, and whether the model involved haploid, diploid or haplo-diploid modes of inheritance, the parameter controlling the rate of dispersal simply cancelled out of the analysis: cooperation evolved just as readily in fully mixing populations as it does in viscous populations (Box 3). Taylor (1992b) followed this analysis with a model of cooperation in a viscous ‘lattice’ population, and again recovered the same result. For reasons that remain somewhat obscure, in an apparently wide class of models the relatedness-enhancing effect of limited dispersal is exactly balanced by the competition -enhancing effect of limited dispersal. The situation is not always so bleak for viscosity and cooperation, however. Haldane (1932) had sketched a model similar to Wright’s in which selection between groups was mediated not by differential production of individual dispersers but by differential production of daughter groups, which compete for living space with other groups. Haldane suggested that if groups are small, then

1 The Evolution and Ecology of Cooperation – History and Concepts

23

Box 3 Impact of rate and pattern of dispersal Rate of dispersal Consider, as Wright (1945) does, that groups are made up of N individuals, and for simplicity we will assume that individuals are haploid and that a single locus controls their cooperation strategy. We begin with a population that is genetically uniform at this locus, and consider the fate of a vanishingly rare mutant allele that subsequently appears and increases the cooperation of its bearers by a small amount. Cooperation incurs a relative fecundity cost C and gives a total benefit B that is shared equally among all members of an individual’s social group (including itself). We assume B, C ⬍⬍ 1. Hence, the relative fecundity of a cooperator in a group containing i cooperators is: fi = 1 + B

i − C, N

(B3.1)

the average fecundity of her group is: fi = 1 + ( B − C )

i , N

(B3.2)

and the fecundity of the average group is: f ≈ 1.

(B3.3)

We now assume that: the offspring disperse to a random group elsewhere in the population with probability d, or else remain on their natal group with probability 1–d; all adults die; and density-dependent regulation returns each group to size N and the juveniles mature to adulthood to take us back to the beginning of the lifecycle. Then, the fitness of the cooperator in the group of i cooperators is: wi = d fi

fi i 1 + (1 − d ) ≈ 1 + ( B − (1 − d )2 ( B − C )) − C. dfi + (1 − d ) f N f

(B3.4)

Denote the expected proportion of cooperators in an individual’s group, averaging over all cooperators rather than over all groups, as R. Hence, the average fitness of a cooperator in this population is: w ≈ 1 + ( B − (1 − d )2 ( B − C )) R − C.

(B3.5)

Note that R is the expected relatedness of an individual to a randomly drawn member of its own group, including itself. Thus, the relatedness between different group mates is r, which satisfies R = (1/N) + ( (N-1)/N)r. Substituting into our expression for the average fitness of cooperators, obtains: (continued)

24

A. Gardner, K.R. Foster

Box 3

(continued)

⎛ B − (1 − d )2 ( B − C ) ⎞ ( N − 1)( B −(1 − d )2 ( B − C )) w ≈ 1− ⎜C − r, ⎟⎠ + N N ⎝

(B3.6)

and since the condition for cooperators to invade is w > 1, this yields Hamilton’s rule, −c + br > 0, where: c=C− b=

B − (1 − d )2 ( B − C ) , N

( N − 1)( B − (1 − d )2 ( B − C )) , N

(B3.7)

(B3.8)

i.e., both the direct and indirect fitness effects of cooperation are modulated by the ecological parameter: the rate of dispersal, d. As Wright (1945) noted, dispersal also impacts on the genetic structure of populations, and this can be shown by calculating the coefficient of relatedness r in terms of model parameters. If we subscript the relatedness coefficient to denote the generation in which we take our measurement, then we can write the following recursion: ⎛ 1 N −1 ⎞ rt +1 = (1 − d )2 Rt = (1 − d )2 ⎜ + rt ⎟ , ⎝N ⎠ N

(B3.9)

because with probability (1-d)2 neither of the two individuals dispersed from its natal group. Solving for equilibrium rt = rt+1 = r, we have: r=

(1 − d )2 , N − ( N − 1)(1 − d )2

(B3.10)

i.e., relatedness is indeed also dependent on the ecology of the population. Note that a very curious result is recovered when we substitute this relatedness expression into our Hamilton’s rule, to derive a condition for increase in cooperation. We obtain: −C +

B > 0, N

(B3.11)

so that although ecology impacts individually upon the cost and benefit and coefficient of relatedness, it does not influence the overall condition for cooperation to be favored. Indeed, in this simple model, cooperation evolves just as readily (or unreadily) in a viscous population as it does in a fully mixing population (Taylor 1992a). It is important to note, however, that how we (continued)

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25

Box 3 (continued) classify this cooperation is dependent on the ecological details. Focusing on the region of parameter space over which cooperation is favored, depending on the rate of dispersal, the cooperation may be altruistic (c, b > 0) or mutually beneficial (c < 0, b > 0) (Rousset 2004). Pattern of dispersal Things are changed somewhat when we consider the effect of varying the pattern of dispersal. The following investigation of ‘budding’ dispersal is based upon the ‘tribe splitting’ model of Haldane (1932) and the analysis of Gardner and West (2006). We begin by making the same assumptions as in the previous individual dispersal model. However, we now assume that, after social interaction has determined individual fecundities: offspring randomly collect together with other juveniles on their patch to form a ‘bud’ of N individuals, which either disperses with probability dB to a random patch, or else remains on the natal patch with probability 1–dB; then all adults die; then of all the buds finding themselves competing for space on a particular patch, one is chosen at random to escape being destroyed by density dependent regulation; and then finally we allow for random exchange of individuals at rate dI between patches. Implementing these assumptions gives a new expression for the expected fitness of a cooperator in a group of i cooperators: wi = dB fi

fi i 1 + (1 − dB ) ≈ 1 + ( B − (1 − dB )2 ( B − C )) − C. dB fi + (1 − dB ) f N f (B3.12)

The new assumptions also impact the recursion for relatedness, r: ⎛ 1 N −1 ⎞ rt +1 = (1 − d1 )2 ⎜ + rt ⎟ . ⎝N ⎠ N

(B3.13)

Following the same procedure as before, we derive a Hamilton’s rule describing the condition for increase in cooperation, −c+br > 0, where: c=C− b=

B − (1 − dB )2 ( B − C ) , N

(B3.14)

( N − 1)( B − (1 − dB )2 ( B − C )) , N

(B3.15)

(1 − d1 )2 . N − ( N − 1)(1 − d1 )2

(B3.16)

r=

(continued)

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A. Gardner, K.R. Foster

Box 3 (continued) Thus, as before, ecology impacts all the components of Hamilton’s rule: budding dispersal, by mediating the degree of kin competition, impacts on the fitness components; individual dispersal, by mediating the genetic structure of populations, impacts upon the coefficient of relatedness. This budding model has decoupled the competition and relatedness effects of dispersal that were bound together in the previous model. Indeed, the budding dispersal model becomes mathematically equivalent to the individual dispersal model when we impose the constraint dB = dI = d. However, in contrast to the individual dispersal model, the condition for increase in cooperation is not generally independent of the ecology, and is given by 1 − (1 − dB )2 B > C. ( N − 1)(1 − (1 − d1 )2 ) + 1 − (1 − dB )2

(B3.17)

In the special case of zero exchange of individuals between groups (dI = 0), equilibrium relatedness is 1 (clonal groups), and this condition for increase reduces to (B–C)dB > 0. Here, so long as there is some relaxation of kin competition due to budding dispersal (dB > 0), then any act that gives a net increase to group fecundity (B–C>0) is favored by selection.

by chance some daughter groups would be more altruistic than others, and this random replenishment of between-group variation would provide a possibility for sustained group selection for altruism. This stochastic ‘tribe-splitting’ model of group selection resisted quantitative exploration, though a simulation study by Goodnight (1992) produced results that seemed to confirm Haldane’s argument, and showed that altruistic cooperation could readily evolve in this model. More recently, Gardner and West (2006) rephrased the model in terms of kin selection, and provided a straightforward analytical treatment of the model and conditions for when cooperation would be favored (Box 3). Thus, the pattern as well as the rate of dispersal has important implications for our understanding of social evolution. Various other ecological and demographic details examined in the context of cooperation in viscous populations include: population elasticity (Taylor 1992b; Mitteldorf and Wilson 2000; van Baalen and Rand 1998); overlapping generations (Taylor and Irwin 2000; Irwin and Taylor 2001); hard versus soft selection (Rousset 2004; Gardner and West 2006); transgenerational cooperation (Lehmann 2007); and catastrophic disturbances (Brockhurst 2007; Brockhurst et al. 2007). An empirical verification of the importance of kin-competition came with the discovery that male fighting in fig wasps is just as brutal in species where the

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27

competitors are highly related, i.e., full brothers, as in species where they are generally unrelated (West et al. 2001). Localized competition in the fig is of an intensity that overrides the relatedness incentive for self-restraint. Similarly, localized competition has been shown to reduce cooperative contribution to public goods in bacteria (Griffin et al. 2004) and humans (West et al. 2006). Such effects have led to the development of a concept of ‘effective’ relatedness. Relatedness is a relative measure of genetic similarity, taken with respect to the population average. However, defining the population is a somewhat arbitrary matter. Queller (1994; and see Kelly 1994) suggested that the effects of kin competition could be subsumed into the coefficient of relatedness by measuring genetic similarity with reference to the ‘economic neighborhood’, i.e., the scale at which competition occurs, rather than the population as a whole. This has proven to be a useful conceptual aid, and leads to the simple idea that as competition becomes more localized, and hence the genetic similarity to one’s competitors increases, the effective relatedness towards one’s social partners is decreased. Thus, as a general rule of thumb, local competition should inhibit the evolution of cooperation. Also, because the effective relatedness can be driven below zero and become negative, local competition should promote the evolution of harmful or even spiteful behaviors (Gardner and West 2004a; Gardner et al. 2004, 2007a). In all of these cases, ecology is the key to making predictions for social evolution.

1.4.3

The Tragedy of the Commons

Another approach that has emphasized ecological aspects of social evolution is theory based upon the analogy of the “tragedy of the commons” (Rankin et al. 2007a). This analogy has its roots firmly in ecology, with a now-famous paper by Garret Hardin in the 1960s, which argued that, without curbs on individual-oriented human behavior, society is heading for ecological disaster (Hardin 1968). The name comes from the analogy of a commons pasture open to many herdsmen, where the best strategy for each herdsman is to add as many cattle as possible, even though this eventually causes the demise of the pasture. The tragedy arises because the benefit of adding an extra cow to the commons accrues only to its owner, while the cost is shared equally amongst all the users of the commons. In evolutionary terms, this is another way of phrasing the problem presented by cooperation, which often involves a tension between the individual and the group (Leigh 1977; Frank 1994, 1995; Foster 2004; Wenseleers et al. 2004b). To a great extent, this is the same problem that Hamilton solved long ago, but the tragedy of the commons analogy has utility because it explicitly describes the performance of the social group (Foster 2006). This has led to a modeling approach based upon neighbor-modulated fitness, but which emphasizes the tension between levels of selection. Notably, Frank (1994, 1995, 1996, 2003) has elegantly modeled the evolution of parasite virulence and policing behaviors by taking a tragedy of the commons approach. In these models, the neighbor-modulated fitness (w) of the individual in a group is

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written as a function of its own selfishness (z) and of the average selfishness exhibited among the members of its group (z′): w ( z, z ′ ) =

f (z) g( z ′ ), f (z ′)

(4.3.1)

where the individual’s relative share f(z)/f(z′) of the group’s success increases with its own selfishness (z) and decreases with the average selfishness of the group (z′), and where the success of the group g(z′) decreases with the average selfishness of its constituent members (z′). Frank (1994, 1995) examined the simple form: w ( z, z ′ ) =

z (1 − z ′ ). z′

(4.3.2)

Using the standard neighbor modulated fitness approach outlined in Box 2, Frank found that the evolutionarily stable level of selfishness is z* = 1 − r. If relatedness is absent (r = 0) then full selfishness (z* = 1) is predicted. However, a degree of relatedness (r > 0) can avert the tragedy, and the group can be expected to enjoy some success (g > 0). The multi-level nature of such models lends them to ecological considerations. Most simply, one can ask how the shape of the within-group (f ) and group-level (g) success functions affects the outcome of social evolution, and in particular, the extent of any social tragedy (Foster 2004). This reveals that the performance of social groups is enhanced whenever investment in either individual competition or, conversely, group-level cooperation provide diminishing returns (successive investments give smaller and smaller increments in reward). The ecology of many social species suggests that diminishing returns will be common, and therefore social tragedy may be typically less pronounced than simple linear models suggest. A nice example is blood sharing in vampire bats whereby the bats give blood to others in the group that did not manage to forage on a particular evening. Here the selfish benefits of holding onto blood diminish with the more blood that is retained as each bat can only use so much, which promotes sharing of at least some blood with the others (Fig. 1.3). Further ecological realism has been built into this approach by models that express within-group and group-level performance as functions of group size, where, following the logic of the tragedy, group size decreases as more competition evolves (Rankin 2007; Rankin et al. 2007a; 2007b). A simple corollary of this is that species with intense competition will have small populations and may even drive themselves to extinction in a process termed ‘evolutionary suicide’ (Rankin and Lopez-Sepulcre 2005). This of course raises the question of why species do not frequently engage in so much competition that they drive themselves extinct. One solution is that the selective incentive for competition is density-dependent such that at low population density, competition is not selected and the species will not evolve the final coup de grace (Rankin 2007). However, it may also be the case that species have frequently driven themselves extinct through this process (Rankin and Lopez-Sepulcre 2005). This raises the interesting possibility for a species-level selection process to favor those species organized in such a way as to remove the selfish incentive that erodes

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Fig. 1.3 Blood sharing in vampire bats as an example of diminishing returns in a social trait (Foster 2004). Consideration of the ecological costs and benefits of blood sharing reveal that very low levels of relatedness are required for blood sharing to function extremely well. a Individual performance function f(z) = 1 – (1 – z)3 based upon the empirically determined relationship between proportion of blood meal retained (investment in self) and time to starvation (Wilkinson 1984), which is used as a proxy for reproductive benefit. The curve closely approximates Fig. 2 in Wilkinson 1984 after the axes have been normalized to a 0 to1 range. b Relationship between investment in reproductive competition and group performance g(z) = 1 – a(z – b)2 where a = 25, b = 0.8. This is based on the observation that around 20% of bats do not feed each night so that the remaining bats will have to donate on average 20% of their resources for all bats to have equal survival probability, which is assumed to maximize group survival. c Investment in reproductive competition at equilibrium (z*) as a function of within-group relatedness. d Group performance at equilibrium g(z*) as a function of within-group relatedness. This predicts how close group performance matches that of a perfectly cooperative group and measures the tragedy of the commons. See Foster (2004) for more details

cooperation (Rankin et al. 2007b), which will moderate the degree of social conflict that we see in nature. Interestingly, this argument, which has its roots in an essay by J.B.S. Haldane (1939), is greatly strengthened when one considers ecological competition among species, because now competitive exclusion means that species even slightly weakened by internal competition can be driven extinct (Rankin et al. 2007b). This observation illustrates how explicit consideration of ecological processes can strongly affect the conclusions of a social evolution model.

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A. Gardner, K.R. Foster

Closing Remarks

Although it has played upon the minds of theoretical biologists ever since Darwin, the ecology of cooperation is far from being properly understood. On the one hand, we have seen that the formal foundations of social-evolutionary theory are well developed and that core results such as Hamilton’s rule provide a conceptually simple but also a completely general framework in which to understand the evolution of cooperation in terms of direct and indirect fitness benefits. On the other hand, it is abundantly clear that the link between an individual’s genes and its inclusive fitness is heavily mediated by ecology. We still have much to understand about these ecological effects, both theoretically and empirically. Like so many topics within evolutionary biology, there is a need for more work that combines theory with careful natural history, but as we proceed, we should remember the extraordinarily prescient work of Kropotkin, the father of ecological sociobiology, and his law of Mutual Aid : “As soon as we study animals – not in laboratories and museums only, but in the forest and the prairie, in the steppe and the mountains – we at once perceive that though there is an immense amount of warfare and extermination…, there is, at the same time, as much, or perhaps even more, of mutual support, mutual aid, and mutual defence…” (Kropotkin 1902) Acknowledgements The authors thank Ashleigh Griffin, Hanna Kokko, Stuart West, Daniel Rankin, and John Koschwanez for helpful discussion. We gratefully acknowledge a Royal Society University Research Fellowship (AG) and a National Institute of General Medical Sciences Center of Excellence Grant (KRF) for funding.

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Chapter 2

The Ecology of Altruism in a Clonal Insect Nathan Pike(* ü ) and William A. Foster

Abstract Social aphids are an ideal animal group in which to demonstrate the relative importance of ecological versus genetic factors in the evolution of sociality for several reasons: (1) Since aphids are clonal, the genetics of a colony is starkly simple (the aphids are either from the same clone or they are not) and, in principle, easy to measure; (2) Because good phylogenies are available for several aphid taxa and there is clear evidence that there have been more independent origins of sociality in aphids than in any other social clade, it is possible to test for associations between ecological factors and the evolution of sociality; (3) Recent developments, in the understanding of the mechanism of the proximate control of soldier development, in the genetic basis of sociality, and in models of social evolution, make the social aphids an ideal group for experimental work on the evolution of social behavior; (4) The social aphids are of special ecological interest because they include the only organisms that have evolved sterile castes in societies that do not occupy some kind of nest (the secondary-host generations of the Hormaphidinae). The ecological context of altruism in social aphids has been shown to be quite intricate since it is now clear that colony defense is not the only costly behavior that they perform: they also have vital roles in keeping the colony clean, migrating to new colonies, and repairing their nest. Numerous ecological factors are highly pertinent in aphid social evolution including (1) the fact that all social aphids have at some stage in their life cycle a valuable and defensive fortress in the form of a plant gall, (2) population size and density, (3) birth rate, (4) the level of exposure to specialized predation, and (5) variation in the level of tending provided by ants. Kin selection in social aphids has given rise not only to a range of elaborate adaptations in behavior and morphology but also to impressive short-term flexibility in social investment. For example, in species that have specialized defenders that can mature to make a direct contribution to their colony’s fitness, defense investment can be increased both through heightened production of defenders at birth and prolongation of the defender stage. Nathan Pike Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK [email protected]

J. Korb and J. Heinze (eds.), Ecology of Social Evolution. © Springer-Verlag Berlin Heidelberg 2008

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We demonstrate that ecological factors are essential in any attempt to understand the role of kin selection in the evolution of social behavior in a group of organisms: ecology determines the extent to which groups consist of related individuals and the context in which these individuals can give and receive help.

2.1

Introduction

Social aphids provide an excellent system in which to study the role of ecology in the evolution of altruism. This is primarily because the other essential component of kin-selected explanations of altruism – relatedness – is straightforward and in principle easy to measure: the aphids in a colony are either from the same clone or they are not. Ecology determines the extent to which colony members are a pure clone and whether social behavior will be selectively advantageous. Aphids are, of course, not the only clonal organisms that are social, and there has recently been an upsurge of interest in the evolutionary biology of these organisms, especially microorganisms (e.g., Crespi 2001; Griffin et al. 2004; Queller 2004), such as bacteria, myxobacteria, and cellular slime moulds, and also higher organisms, such as marine invertebrates and polyembryonic wasps (Cruz et al. 1990; Duffy et al. 2002). The social aphids stand out from these other clonal organisms because they consist of clones whose members are highly mobile and independent of each other and also because we have far more reliable information about their phylogeny, their ecology and their genetic structure. However, the general ideas that we are discussing here are relevant to our understanding of the evolutionary biology of a very wide range of events from the origins of multicellularity to social interactions in bacteria. In this chapter, after a very brief introduction to the biology of social aphids, we will discuss developments in our understanding of their social evolution since the reviews of Stern and Foster (1996, 1997). Hamilton (1964) was the first to point out the paradox of the rarity of altruism in clonal organisms in general and in aphids in particular. In these organisms, any helping behavior that reaps more rewards than it costs will be selected for. The paradox is more apparent than real: altruism is in fact quite common in clonal organisms, if we relax the definition to include multicellularity. Even in aphids, social behaviors have evolved independently on many occasions: possibly as many as 17 times (Fukatsu, pers. comm.), considerably more than in any of the other major taxa of eusocial insects. In addition, the conditions favoring the evolution of altruism remain quite stringent, even in clonal organisms. An individual’s critical cost/benefit ratio (i.e., direct offspring lost through altruism/indirect offspring gained through altruism) of unity is no lower than in societies of diploids or haplodiploids ruled by a singly mated queen, and the issue of the maintenance of clonal purity is crucial. The chief reason given by Hamilton (1972) for the absence of social aphids is almost certainly wrong, namely that

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there is little scope for providing help if you are a specialized sedentary sapfeeder. Recent work has demonstrated the inexhaustible inventiveness of natural selection in providing ways in which these small sapsuckers can help each other (see Sect. 2.4).

2.2

Basic Biology of Aphid Soldiers

Aphids are small, phloem-feeding bugs (Order Hemiptera; Suborder Sternorrhyncha), which, for most generations, are parthenogenetic and bear live young. In most species, a series of parthenogenetic generations alternates with a single generation of sexual reproduction. A minority of aphid species (about 10%, but including almost all the social species) alternate between two plant species: the primary host, where sex occurs and several parthenogenetic generations are produced, and a secondary host where successive entirely parthenogenetic generations of females develop. The most widespread feature of aphid sociality is the presence of soldiers that defend the clone against predators. These soldiers are almost always early instars, although there is one example of an adult aphid showing defensive behavior (Inbar 1998). The soldiers are impressively diverse, both in morphology and physiology. The commonest weapons are highly sclerotized stylets, legs and horns, and some soldiers are known to inject venomous proteases. The only way to study the behavioral subtleties of caste in aphids, as for all social insects, is by detailed observations, and recent studies have suggested that aphids might have unexpectedly complex caste systems to rival those of the social Hymenoptera. Rhoden and Foster (2002) studied six species of Pemphigus and showed that defensive behavior was widespread not only among the different Pemphigus species, including those without any morphological specialization, but also among the different developmental stages. First instars were always the most aggressive, but later instars in all the soldier-producing species showed some degree of antipredator behavior. These observations suggest that defensive behavior might be quite widespread and generalized in this genus, and can be adapted flexibly in response to the ecology of a particular species. In two sibling species of Pseudoregma that produce dimorphic first-instar larvae of soldiers and non-soldiers, Shingleton and Foster (2001) showed that the division of labor in these larvae could be very flexible, with non-soldiers frequently being recruited into defensive roles. There are essentially two axes along which aphid soldiers can be aligned: sterility and morphological specialization. At one extreme are highly specialized, obligately sterile first instars, which never moult to the next instar. These would include Pseudoregma alexanderi soldiers on the secondary host (Aoki and Miyazaki 1978). At the other extreme are those soldiers, for example early instar gall-generations of Pemphigus bursarius, that are not morphologically specialized

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and all have the potential to develop into winged individuals that fly from the gall. The intermediate phenomenon of facultative sterility is also well known. Some soldiers have the potential to mature to adulthood despite also being physically specialized, but their development may be delayed to such an extent that they do not, in practice, have much chance of reproducing. This is the case for the third-generation soldiers of Pemphigus spyrothecae (Pike et al. 2004; Rhoden and Foster 2002). We follow Stern and Foster (1997) in classing all the defensive aphid morphs as “soldiers” and not restricting the term just to those morphs that are obligately sterile.

2.3

The Phylogenetic Distribution of Aphid Soldiers

Of the approximately 4,700 species of aphids described (Remaudière and Remaudière 1997), around 60 are known to be social. These social species are found in six tribes: the Pemphigini, Eriosomatini and Fordini of the Pemphiginae and the Hormaphidini, Certataphidini and Nipponaphidini of the Hormaphidinae (Fig. 2.1). The fact that aphid sociality is evolutionarily labile is evident even from examination of phylogenies providing only subfamily/tribe resolution. For example, the asocial Thelaxinae and Anoeciinae occur deep amongst the lineages in which some of the most social species occur (Ortiz-Rivas et al. 2004). More significantly, because the degree and, in many cases the presence, of sociality varies within each of the soldier-producing tribes, it is clear that soldiers have evolved and been lost a number of times. For example, in the Cerataphidini, while soldiers are always present in primary-host colonies, Stern’s (1998) examination of secondary-host soldiers indicates that these specialized horned defenders have evolved once and been lost once or twice. At the level encompassing all taxa known to contain social species, Stern and Foster (1996) gave a highly conservative early estimate of six to nine origins but Fukatsu (pers. comm.) has good evidence that the soldiering trait has evolved at least 17 times. These figures dwarf the number of independent origins of sociality found in other taxa such as the wasps, bees and termites. Of the 17 evolutionary origins estimated by Fukatsu, four or five have produced extreme cases in which there is absolute division of labor between reproductives and sterile soldiers. The number of losses of aphid sociality is more difficult to estimate accurately because detailed behavioral observations are lacking for many pemphigine and hormaphidine species. It is nevertheless clear that these evolutionary losses are also numerous. The six aphid tribes named above provide biologists with one of the few social clades for which a good phylogeny is available (see also Chap. 3 for thrips). By also being a unique clade for having had multiple losses of social traits in diverse lineages, these aphids provide a unique opportunity for understanding the determining influence of ecology on sociality.

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2.4

41

Are Aphids Eusocial?

It has not been universally accepted that the soldier-producing aphids are eusocial (e.g., Gullan and Cranston 1994; Hölldobler and Wilson 1990). This seems unreasonable, since many species readily fulfill the three traditional criteria of eusociality. All aphids routinely show overlap of generations and those with sterile soldiers clearly have reproductive division of labor. The sticking point would seem to be cooperative brood care, but recent work has clearly shown that many species show an intricate range of cooperative behavior, principally to do with the care and maintenance of the “fortress” (the plant gall). We discuss these behaviors here, not primarily in defense of the aphids’ eusociality, which is largely a matter of semantics, but because of the light they throw on the complex ecological context of altruism in these animals.

Fig. 2.1 A molecular phylogeny for selected species from family Aphididae based on variation of the DNA sequence of the long-wavelength opsin gene. Species names are given along with tribes (where possible) and subfamilies. Tribes and subfamilies known to contain social species are indicated in bold. Vertical lines (or, in the case of the apparently polyphyletic Eulachnini, asterisks) indicate multiple members of a higher taxon. Bootstrap support for maximum likelihood analysis is indicated above branches and, for values of 50 and greater, bootstrap support for maximum parsimony analysis is indicated below branches. Bootstrap values derived from analysis of first-plussecond positions only are given to the left of the slash and those derived from analysis of all positions are given to the right. Three main clades are apparent (indicated by the letters A–C), with all known social aphids occurring in clade A. The value in parentheses indicates the bootstrap value obtained in a maximum parsimony combined analysis of the long-wavelength opsin sequences and mitochondrial ARP-6 sequences (modified from Ortiz-Rivas et al. 2004, with permission)

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Colony Defense

The unique behavioral, morphological, and physiological adaptations associated with defense are perhaps the best evidence of advanced social specialization (Stern and Foster 1996, 1997). The weaponry used by aphid soldiers against their predators is hugely diverse, including the following combinations: stylet with hindlegs (e.g., Pemphigus spyrothecae, Foster 1990), stylet with fore and mid legs (e.g., Colophina clematis, Aoki 1977), stylet alone (e.g., the primary host soldiers of Pseudoregma bambicicola, Aoki and Kurosu 1992a), horns and forelegs (e.g., Pseudoregma alexanderi Aoki et al. 1981). The soldiers of Tuberaphis styraci manufacture a highly toxic protease that is injected through their stylets into predators (Kutsukake et al. 2004) and it is likely that a number of other aphid soldiers use venom in a similar fashion. Although adult and larval predators that are attacking the colonies are the usual targets for soldier defense, eggs are sometimes attacked preemptively (e.g., Ceratovacuna lanigera, Aoki et al. 1984), just as preemptive patrolling of the exterior of the gall is also known (e.g., Ceratovacuna nekoashi, Kurosu and Aoki 1988). Although defense usually falls to the first instars (e.g., Hamamelistes cristafoliae, Akimoto et al. 1996) or second instars (Tuberaphis styraci Aoki and Kurosu 1989a), this is not prescriptive and defense is also known in the third instar (e.g., Eriosoma moriokense, Akimoto 1983; some Pemphigus spp., Rhoden and Foster 2002), the fourth instar (Grylloprociphilus imbricator, Aoki et al. 2001) and even in adults (Smynthurodes betae, Inbar 1998).

2.4.2

Gall-Cleaning

Soldiers take on a cleaning role by removing honeydew, exuviae and other detritus from the gall in a number of species including Pemphigus dorocola (Aoki 1980), T. styraci (Aoki and Kurosu 1989a) and P. spyrothecae (Benton and Foster 1992; Pike et al. 2002; Fig. 2.2a). It is clear that cleaning can evolve in the absence of any defensive role, as the first instars of Hormaphis betulae, a species without soldiers, cooperate to push large masses of honeydew out of their galls (Kurosu and Aoki 1991). Such cleaning behaviors are costly both in terms of time and energy expenditure but also because it places the individuals near to the gall opening, the site most susceptible to predation. The critical benefits of cleaning are that the potentially devastating microbial and fungal pathogens are deprived of the honeydew on which they thrive and the full volume of the gall can be used by the aphids.

2.4.3

Intergall Migration

Because survival outside of a colony is exceedingly poor, altruistic migration by soldiers away from the native clone to invade an alien colony is a high-risk behavior. Nevertheless, it is also a behavior that can pay huge dividends in terms of reproductive

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a

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b

Diameter of honeydew ball (mm)

1.0

10 27 26 26 12 17 15 527 39 10 27 23 17 27

0.9

Clonal proportions

0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0

Cleaning method

c

A B C D E F G H I

J K L M N

Gall

d

10 mm

0.1 mm

Fig. 2.2 Some lesser-known altruistic behaviors of social aphids. a The diversity of cleaning behaviors seen in P. spyrothecae. The method of removal of wax-coated balls of liquid honeydew is modified according to the size of ball to be removed, with the possible exception of the ‘kick’ and ‘back’ behaviors, which were both used for the smallest balls. The number of observations of each behavior is given above the x-axis (from Benton and Foster 1992, with permission). b Clonal mixing, the outcome of migration, in P. spyrothecae. Microsatellite genotyping of the number of individuals given above each bar was used to identify the proportion of different clones in 14 discrete galling colonies (marked A-N ). These results are discussed in an earlier section. (modified from Johnson et al. 2002, with permission). c Gall repair in P. spyrothecae. A square hole has been cut in the gall on the left. The full repair seen in the gall on the right is achieved over several days during which the aphids induce compensatory growth into the hole from an undamaged portion of the gall. d Soldiers of Astegopteryx spinocephala cooperating to seal the opening of their subgall with their spinous heads (from Kurosu et al. 2006b, with permission)

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success. Alien individuals certainly occur in apparently closed colonies (Johnson et al. 2002, Fig. 2.2b) and there is good reason to expect that migration is widespread (Aoki 1982). It has been documented for Pemphigus obesinymphae that these payoffs can be maximized because the migrating soldiers ‘cheat’ by hastening development and abandoning defensive behavior once they have successfully colonized a gall established by an alien clone (Abbot et al. 2001; and see Sect. 2.6).

2.4.4

Gall-Repair

As the gall represents a resource-rich fortress that protects the colony from predators (Sect. 2.7.1), prompt repair of any breech in the fortress’s walls will be under strong selection. In P. spyrothecae, the aphids induce this repair by stimulating the host plant to create complementary regrowth in the gall to fill the damaged area (Pike and Foster 2004, Fig. 2.2c) and, more remarkably, in Nipponaphis monzeni, soldiers rapidly seal over holes in their gall by exploding their bodies to release a viscous fluid in which they fatally entrap themselves (Kurosu et al. 2003). Although it has not been studied in detail, highly effective gall repair is also known to occur in Ceratoglyphina bambusae (Aoki and Kurosu 1991). As in P. spyrothecae, this repair apparently occurs relatively slowly, relying on the aphids’ manipulation of the plant tissue of their damaged gall.

2.4.5

Blocking Behavior

In Astegopteryx spinocephala, a less extreme but equally effective method of filling gall openings is employed: soldiers form a group and protrude their specialized spinous heads into the hole to block it entirely (Kurosu et al. 2006a, 2006b, Fig. 2.2d).

2.5

Proximate Factors in the Determination of Soldier Aphids

While investment in defense is known to vary greatly both within and among species, the proximate causes of this variation are, in general, poorly known. Predation (Shibao 1998), population size (Shibao 1999a), seasonal change (Sunose et al. 1982), condition of the host plant (Sakata et al. 1991), and size of the interior surface area of the gall (Stern et al. 1994) have all been proposed, but not substantiated in conclusive manipulative experiments, as proximate cues. One of the first proximate cues for increased investment in soldiers was discovered by deduction. Withgott et al. (1997) found that, in Pemphigus obesinymphae, the death of the founding female of the gall (the fundatrix) resulted in accelerated development of the first instar soldiers into reproductives. Maternal presence, for at least one species, is thus a proximate cue to continued defense investment.

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The difficulty in identifying proximate cues for defense is partly due to the problem that observations and experiments must mostly be done in uncontrolled natural conditions. Shibao et al. (2002) solved this problem for T. styraci by establishing an artificial diet on which the species could be reared in continuous laboratory culture. Shibao et al. (2004a) went on to demonstrate that increased density of aphids in the gall (as distinct from high population size) is the major proximate factor causing an increase in soldier number. This finding was consolidated by examination of soldier proportions in field-collected colonies at high population density. The timing of this density-induced defense investment has also been investigated (Shibao et al. 2003). High aphid density was found to have a prenatal influence on embryos still within the ovarioles of their mothers, which resulted in increased soldier production. Furthermore, the flexibility inherent in having second-instar soldiers was also demonstrated in the finding that postnatal exposure (during the first instar) to high aphid density was also sufficient to induce soldiers. The combination of both pre- and postnatal exposure had a synergistic effect, which resulted in soldier production that was approximately four times greater than highdensity exposure at just one of the two periods. These findings seem to agree with the report of Ijichi et al. (2004) that showed that for Pseudoregma bambucicola, the path to becoming a soldier has two distinct phases: differentiation as an embryo followed by rapid growth after birth. Because the increase in soldier proportion with aphid density tends to reach a plateau in T. styraci colonies under natural conditions, Shibao et al. (2004b) also sought a further regulating mechanism for soldier production. They were able to demonstrate conclusively that soldier number was up-regulated when a low proportion of soldiers is present but down-regulated when the proportion of soldiers is already high (i.e., at around 50%). Caste ratio is thus another proximate factor that can influence defense investment. Clonal mixing (Abbot et al. 2001) and ant tending (Shingleton and Foster 2000) are also documented influences on soldier production but these are dealt with in detail in Sects (2.)6 and (2.)7.3.

2.6

A Genetic Factor in the Evolution of Social Aphids: Clonal Mixing

Clonality is often cited as a fundamental pillar of the evolution of the extreme aphid altruism that is sometimes observed (e.g., Krebs and Davies 1993) and it has been claimed that that the relatedness value of 1 often seen in aphids is the ultimate predisposition to altruism. However, the rarity of social aphid species (which represent just 1% of aphids) provides a clear demonstration that clonality alone is not sufficient to produce altruism (Stern and Foster 1996). The co-requisite ecological factors that encourage altruism by assisting the preservation of monoclonal colonies are discussed in later sections. Clonal mixing, a genetic consideration that can undermine the benefits of altruism, is discussed here.

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Hamilton (1987) recognized the potential for aphids from one clone to invade and steal the altruism of another clone, calling the invaders “self-propelled cuckoo eggs”. The benefits of invading a social aphid colony are clear: the invader gains from its host’s food and protection and is relieved of the genetic obligation to perform altruistic duties. The major gain for the invader’s clone is that the clonal genotype is destined to propagate safely in a second location and thus serve as a hedged bet in the event of a calamity befalling the home colony. The only risk incurred when seeking this benefit from invasion is that the invaders may not find a host colony, but this risk can be somewhat alleviated if the invaders are individuals with relatively low reproductive value. As early as 1980, Setzer used allozyme analysis to demonstrate that colonies of Pemphigus populitransversus routinely contain up to 25% invaders. Perhaps tellingly, this species is not known to be social although it is closely related to numerous species that are. In P. spyrothecae, a species which is highly social, microsatellite genotyping has been used to demonstrate that the average level of clonal contamination was 10%, albeit with a great range that varied from 0–59% (Johnson et al. 2002). In around 2% of colonies, this contamination was due to multiple alien clones. In one case, nine alien clones were found in a colony that was only 2% contaminated. This detailed information on clonal mixing may indicate that a very low level of mixing is required to take advantage of the bet-hedging mentioned above. In the case of P. spyrothecae, the scarcity of would-be immigrant cheats associated with low clonal mixing may have played an important part in maintaining the selective advantages of altruistic traits and facilitating the evolution of sociality. In another Pemphigus species, which is highly social, P. obesinymphae, the average level of clonal mixing is 41% with a range of 21–71% (Abbot et al. 2001). Abbot et al. were also able to confirm theoretical predictions by demonstrating that the invaders had (1) a vastly reduced propensity to defend and (2) developmental rates that were accelerated such that they reached the reproductive stage more quickly than individuals of the host clone. At high levels of clonal mixing such as those reported for P. obesinymphae, it becomes reasonable to ask why social behavior persists. Certainly, cheating such as that described might be expected to rapidly erode the evolutionary advantages of altruistic behavior when more than 50% of a colony’s population routinely comes from alien clones. Because natural selection has required similar characteristics from invaders and defenders (e.g., low reproductive value to minimize the loss incurred through risky activities, high cuticular sclerotization as armor or protection against desiccation), the invading individuals may be the same individuals that would be defending were they still in their native clone. The effect of this binding social behavior and invasive behavior in positive feedback may be that higher levels of invasion can be tolerated by native clones (see also Foster 2003). Because clonal mixing has the potential to undermine the benefits conveyed by social behavior, the possibility of social policing to prevent invasion by alien clones has been propounded. A prerequisite to such policing, the ability to distinguish between kin and non-kin, has been assessed in a number of aphid species. Kin recognition was sought, but not found, in C. bambusae (Aoki et al. 1991; Aoki and Kurosu 1991). Instead, it was found that, at the beginning of the galling season, the

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obligately sterile soldiers defended the exterior of their native gall against non-soldier conspecifics, regardless of whether these conspecifics were from the native or an alien clone. By the end of the galling season, this attacking behavior, based on the ability to discriminate soldiers from non-soldiers had disappeared, presumably because the threat of exploitation by fecund individuals was assuaged by the fact that the reproductives were about to disperse. As in C. bambusae, no evidence for kin recognition was found in Ceratovacuna japonica (Carlin et al. 1994) or Pseudoregma bambucicola (Shibao 1999b). Prevention of invasion by alien clones through behavioral means has thus not been found to date. In contrast, the physical barriers to clonal mixing are obvious and effective. These are described in the next section.

2.7

Ecological Factors in the Evolution of Social Aphids

By way of preface to this section in particular, it is worth mentioning that studies of ecological (and genetic) influences upon aphid sociality have focused on defense. Although this focus may sometimes have meant that other social traits were neglected, we hasten to point out that defense is certainly the central social trait that may commonly have been a necessary precursor to the evolution of the others discussed above. In addition, one might reasonably expect that trends in defensive characteristics may often serve at least as qualitative indicators for trends in other social characteristics. For these reasons, the latter parts of this section are mostly devoted to observed and predicted strategies of defense investment. A clear statement of the routes to increased defense investment may thus be subsequently useful: an aphid colony can increase defense by (1) producing a greater number of defenders, (2) lengthening the duration of the defensive stage, (3) improving the efficacy of defense, and/or (4) increasing the plasticity of defensive behavior. We also note that, for reasons which include social aphids’ relatively recent discovery and limited economic importance, direct observations and ecological experiments are entirely lacking for the vast majority of species. Much of the research that relates generally to environmental, life-history and host-related factors is theoretical. Of course, we look forward to a time when empirical evidence to support or refute these predictions becomes available.

2.7.1

Galls

One of the key correlates of aphid sociality is the galling habit. Whereas not all gall-forming aphids are social, all of the approximately 60 aphid species that are known to be social do form galls on a host plant at some point in their life cycle (Foster and Northcott 1994). It thus follows that galling life must convey crucial selective predispositions to sociality, over and above its more general selective advantages (described in detail by Price et al. 1987). The implications that the galling habit holds for the evolution of sociality have been reviewed in detail by Foster and Northcott (1994) and are discussed here only in brief:

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Fortress Defense Queller and Strassman (1998) use the term ‘fortress defense’ to describe the evolution of sociality through selection for group cooperation in exploiting and protecting a rare and valuable habitat. Because galls are a rich and truly invaluable resource to the aphids which create and inhabit them, they are ideal examples of defense-worthy fortresses. Facilitating Anti-Predatory Behavior Besides providing an environment that is worthy of defense, the gall also serves as a readily defensible fortress in that, for the vast majority of its surface area, it represents a physical barrier to predation. If only the points of entry require active monitoring and defense, the behavioral effort and increased morphological specialization requisite to effective social defense may be reduced to a level that is not only selectively tenable but, indeed, favorable. Specialized placement of morphs within the gall has been demonstrated in P. spyrothecae. Soldiers tend to inhabit the area of the gall closest to the opening whereas reproductives (sexuparae) tend to inhabit the area of the gall furthest from the opening (Pike 2007). Encouraging Clonal Integrity If defense and other altruistic traits are to produce fitness benefits for the genotypes that invest in them, it is paramount that the individual beneficiaries belong to the same clone. The possibilities for cheating through clonal mixing were discussed in section 0. Such cheating, if sufficiently common, would certainly result in the total breakdown of altruism. However, galls also provide barriers to invasion by alien aphids and, in doing so, preserve the intense potential for intra-clonal selection to promote altruism. The pivotal role the gall has in encouraging defense is also manifest in comparisons among species (Pike 2002; Rhoden and Foster 2002) and in theoretical findings (Akimoto 1996; Pike and Manica 2006a) which indicate that, as duration of the galling stage increases, so too does the degree to which soldier production is favored.

2.7.2

Life-History and Host Variables

Birth Rate Numerous theoretical studies have set out to elucidate the conditions that encourage increased investment in defense. One of the notable conclusions from the earlier studies (Akimoto 1996; Stern and Foster 1996) was that low colony birth rate would favor soldier production. The biological rationale for this mathematical conclusion is that defense is most important for populations that are least able to replace individuals lost

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to predation. Increasing the number of soldiers born is perhaps the most obvious way to increase defense. We know that in species with dimorphic nymphs soldiers are certainly distinguishable from non-soldiers immediately from birth, and recent studies of embryology and ontogeny confirm that the allocation decision can be made considerably earlier (Ijichi et al. 2004). In both Colophina arma and P. bambucicola, soldier differentiation is initiated during embryogenesis (Ijichi et al. 2005). However, in C. arma (the species with more specialized soldiers), this differentiation occurs much earlier than it does in P. bambucicola.

Colony Size, Growth Rate, and Carrying Capacity of Host A series of investigations has assessed the basis of the tendency for larger colonies to have greater proportions of soldiers. This tendency has been empirically sought in a number of species with obligately sterile soldiers and there is evidence for its occurrence in P. bambucicola (Itô et al. 1995; Shibao 1998) and P. sundanica (Schütze and Maschwitz 1991; Shingleton and Foster 2001). Aoki and Kurosu (2003) created a logistic population model which is consistent with the densitydependent declining growth rate that is expected to differing degrees in both galldwelling and free-living aphid colonies. The model of Aoki and Kurosu (2003) indicated that production of soldiers should be more easily favored in large colonies than in small ones. The reason for this effect was that because the fitness impact of a soldier’s defensive efforts is greatest in populations near carrying capacity, its indirect fitness contribution to its colony was most likely to outweigh the limited direct contribution that the presence of another reproductive would produce. The authors were quick to point out that the rate of colony growth was also predicted to have a marked effect on propensity to soldier production, with faster-growing colonies likely to have less impetus to produce soldiers. Expanding on their previous model, Aoki and Kurosu (2004) pointed out that because defense by soldiers increases the intrinsic growth rate of an aphid population, the presence of soldiers allows for a larger optimal colony size than would otherwise be expected. They were also able to determine that the optimal number of soldiers could be calculated by determining up until what point the defensive efficacy resulting from the production of another soldier ceases to exceed rm/K, the ratio of the colony’s intrinsic growth rate and the theoretical carrying capacity. Interestingly, they predicted that this optimal number was the same regardless of whether the aphid colony was monoclonal or polyclonal. A colony made up of multiple genotypes was, however, expected to conform to Hamilton’s Rule by having a larger overall population size and, consequently, a lower proportion of soldiers and a lower productivity than a pure clone. In the most recent model, Aoki and Imai (2005) sought to clarify whether, in larger colonies, there is a demographic expectation of higher proportions of soldiers (in addition to the greater ease of soldier production which had already been demonstrated). Perhaps obviously, soldier proportion was predicted to increase with predation pressure but, beyond this effect and even when the number of predators per

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aphid was constant, the proportion of soldiers increased with increasing colony size. It was also demonstrated that the proportion of soldiers in a mature colony with a small carrying capacity would be greater than the proportion of soldiers in an identically sized developing colony with a high carrying capacity. An elaboration on this finding was the conclusion that under the right conditions (of sufficient limitation by very small carrying capacities), soldierless colonies (such as those recorded by Itô et al. 1995) are the natural outcome of internal population regulation and are not due to external influences such as predation. The positive effect that the aforementioned population parameters had on soldier production was further enhanced under the credible assumption that soldiers incur fewer energetic and material costs than non-soldiers. The state-dependent dynamic model of Tyerman and Roitberg (2004) concurred with earlier authors that defense investment should have an inverse relationship with productivity. In contrast to previous findings, the model was said to predict a negative correlation between soldier proportion and colony size. This contrary prediction was attributed to the expectation that, whereas predators were able to gauge the colony size of the free-living species, they were not able to do so in the case of the galling aphid species. It deserves to be noted, however, that the high proportion of soldiers expected in small colonies dipped only for colonies of intermediate size before rising again for large colonies which had reduced productivity due to reproductive constraints imposed by a looming carrying capacity. The predictions of this model are thus not actually dissimilar from those of other models. In any case, although the link between colony size and soldier proportion may be common, it is probably not a universal rule: for example, empirical evidence collected by Stern et al. (1994) for Cerataphis fransseni suggests that soldier proportion scales with the physical dimensions of the gall.

Aphid Density Section 0 has detailed how aphid density is the major colony-determined proximate cue for soldier production. High density and not large colony size is the trigger for production of more soldiers in T. styraci and (bearing in mind the absence of any obvious mechanisms for an aphid to estimate population size directly) is also a likely trigger for many other species (Shibao et al. 2004a). High density, in the case of galling aphids, effectively means crowding, and this crowding may be the most reliable indicator a colony has when deciding whether increased production of soldiers is necessary and sufficiently cheap.

Colony Lifetime In addition to increasing the proportion of soldiers produced at birth, other forms of defense investment have been examined through models. Pike and Manica (2006b) suggested that soldier behavior may become more risk-averse when

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reproductive rates are low and colony lifetimes are long (i.e., at a time when soldiers are especially costly to replace). Perhaps unexpectedly, this strategy, which amounts to “living to fight another day”, was most favored when predation was high. Lengthening of the defensive instar has been demonstrated in natural populations of both monomorphic Hemipodaphis persimilis (Akimoto 1992) and dimorphic Pemphigus spyrothecae (Pike et al. 2004). This phenomenon, termed instar extension, is thought to be most likely to occur in colonies with long lifetimes (Akimoto 1996) and at times (usually the terminal colony stages) when birth rate is at its lowest. Pike and Manica (2006a) predict that both period and level of exposure to predation are important critical factors which, in conjunction with birth rate, may set the optimal level of defense investment. A further conclusion is that increased soldier production at birth is most likely to be favored when soldiers have a markedly higher rate of mortality compared to non-soldiers. However, these authors’ model also highlighted that flexibility in birth allocation of soldiers was usually not crucial when other methods of increasing defense investment were available.

2.7.3

External Effects

Predation Defense is the aphid’s main answer to predation. Because defense is costly to an aphid colony, variation in predation will exert a selective effect on defensive behavior and morphological traits. Nevertheless, the presence of a plastic response to variation in predation has been neither directly observed in nature nor empirically demonstrated. This lack of demonstrable causality is mostly due to difficulties in assessing predation pressure and is not evidence that an effect is absent. Theoretical approaches that are subject to no such practical constraint have clarified the conditions under which predation may have markedly different effects. The most obvious effect of predation is that, as it increases, so too will the degree to which investment in defense is favored (Akimoto 1996; Aoki and Kurosu 2003; Stern and Foster 1996; see also Chap. 6 on ants). However, if a colony is faced by a “non-gluttonous” predator that eats only a set number of aphids in a given period, one can expect the proportion of soldiers to reach a peak at intermediate colony size and subsequently decrease as the population increases further (Aoki and Imai 2005). The statedependent model of Tyerman and Roitberg (2004) even predicts that for galling aphids, soldier allocation may sometimes be lower when a predator is present in their gall. This prediction was based on the implicit assumption that the predator could serve as a culling influence, which would release the aphids from their densitydependent reproductive constraints. Once thus released, the best strategy for a colony may be to out-reproduce a predator’s limited appetite rather than opting for stubborn and costly defense. The above predictions, which require conservative predation, do not concur with observations that some predators routinely decimate galling colonies (Foster 1990).

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Ant Tending The first demonstration of social aphids’ adjusting their defense investment in response to the environmental change dealt with the case of ant tending (Shingleton and Foster 2000). The authors demonstrated that in the obligatorily ant-tended species Pseudoregma sundanica, the proportion of soldiers increased in colonies that were deprived of ants. It is known that ants actively remove predators from the colonies that they tend (Schütze and Maschwitz 1991) and, because of this, ant tending is likely to serve to some degree as a substitute for defense investment. A subsequent comparative study of P. sundanica and the closely related Pseudoregma nicolaiae supported this conclusion (Shingleton and Foster 2001). It was found that P. nicolaiae, which is rarely ant-tended, had less morphological specialization between soldiers and non-soldiers but that both of these castes were more aggressive than their P. sundanica counterparts. The soldiers of P. nicolaiae were also found to be significantly bigger than the soldiers of P. sundanica. One would expect that the absence of ant defenders might require P. nicolaiae to have a defensive strategy, which involves a stronger first line of specialized defenders as well as non-specialized reinforcements that could defend when sudden changes in circumstances demanded it. The above observations are consistent with this expectation.

2.8

Conclusions

It is clear that the importance of relatedness has been overemphasized in many studies of social evolution – especially in the social insects. This is partly because relatedness is relatively easy both to define and to measure but also because of the seductive complexity inherent in the reproductive asymmetries of the social Hymenoptera. However, although relatedness is clearly an essential component of any kin-selected explanation of sociality, it would be foolish to suggest, as some have done, that there should be any simple relationship between levels of relatedness and eusociality. In essence, relatedness merely sets the threshold that must be overcome by the ecological determinants of the costs and benefits of helping. In probably all social animals, it is the ecological context that drives the evolution of altruism. The social aphids make this point rather clearly. All aphids have what seems like a strong genetic predisposition to help, since they are potentially interacting within a single clone, but yet social aphids are rare. The critical factors that determine whether sociality evolves are to do with the ecological context that affects both the level of clonal purity and the costs and benefits of helping. In conclusion, we would like to point out a gap in our knowledge of aphid soldiers. Although far from comprehensive, our understanding of the biology of gall-dwelling aphid soldiers on the primary host is considerably greater than our understanding of free-living secondary-host soldiers. There is substantial evidence that primaryand secondary-host soldiers are not homologous and that secondary-host soldiers probably evolved more recently (Aoki and Kurosu 1989b; Fukatsu et al. 1994;

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Stern 1998). Secondary-host soldiers are also even rarer than primary-host soldiers. Interestingly, cladistic analyses of these secondary-host soldiers have provided us with one of the most tangible correlations we have for the loss of defense. The switch from bamboos to grasses as secondary hosts is associated with the loss of soldiers (Stern 1998). One possible reason for this evolutionary association is, because grasses may provide better, more accessible nutrition, they may permit the aphids they host to shift their life-history strategy away from defense in favor of rapid reproduction. We know that, in the species where they persist, secondary-host soldiers can defend and migrate between their colonies, but these aphids are the only social animals that have no nest, no home, no fortress. Who knows what novel adaptations, what entirely new behavior, this unique ecological circumstance might have engendered?

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Kurosu U, Aoki S (1991) Gall cleaning by the aphid Hormaphis betulae. J Ethol 9:51–55 Kurosu U, Aoki S, Fukatsu T (2003) Self-sacrificing gall repair by aphid nymphs. Proc R Soc Lond B (Suppl) 270:S12–S14 Kurosu U, Buranapanichpan S, Aoki S (2006a) Astegopteryx spinocephala (Hemiptera: Aphididae), a new aphid species producing sterile soldiers that guard eggs laid in their gall. Entomol Sci 9:181–190 Kurosu U, Narukawa J, Buranapanichpan S, Aoki S (2006b) Head-plug defense in a gall aphid. Insectes Soc 53:86–91 Kutsukake M, Shibao H, Nikoh N, Morioka M, Tamura T, Hoshino T, Ohgiya S, Fukatsu T (2004) Venomous protease of aphid soldier for colony defense. Proc Natl Acad Sci USA 101:11338–11343 Ortiz-Rivas B, Moya A, Martinez-Torres D (2004) Molecular systematics of aphids (Homoptera: Aphididae): new insight from the long-wavelength opsin gene. Mol Phylogenet Evol 30:24–37 Pike N (2002) Defence investment and altruism in Pemphigus Aphids. PhD Thesis, University of Cambridge, Cambridge Pike N (2007) Specialised placement of morphs within the gall of the social aphid Pemphigus spyrothecae. BMC Evol Biol 7:18 Pike N, Foster WA (2004) Fortress repair in the social aphid species, Pemphigus spyrothecae. Anim Behav 67:909–914 Pike N, Manica A (2006a) The optimal balance of defence investment strategies in clonal colonies of social aphids. Behav Ecol Sociobiol 60:803–814 Pike N, Manica A (2006b) The basis of cowardice in social defenders. Ecol Model 196:275–282 Pike N, Richard D, Foster WA, Mahadevan L (2002) How aphids lose their marbles. Proc R Soc Lond B 269:1211–1215 Pike N, Braendle C, Foster WA (2004) Seasonal extension of the soldier instar as a route to increased defence investment in the social aphid Pemphigus spyrothecae. Ecol Entomol 29:89–95 Price PW, Fernandes GW, Waring GL (1987) Adaptive nature of insect galls. Environ Entomol 16:15–24 Queller DC (2004) Kinship is relative. Nature 430:975–976 Queller DC, Strassmann JE (1998) Kin selection and social insects. Bioscience 48:165–175 Remaudière G, Remaudière M (1997) Catalogue des aphides du monde. INRA, Paris Rhoden PK, Foster WA (2002) Soldier behaviour and division of labour in the aphid genus Pemphigus (Hemiptera: Aphididae). Insects Sociaux 49:257–263 Sakata K, Itô Y, Yukawa J, Yamane S (1991) Ratio of sterile soldiers in the Bamboo Aphid, Pseudoregma bambucicola (Homoptera: Aphididae), colonies in relation to social and habitat conditions. Appl Entomol Zool 26:463–468 Schütze M, Maschwitz U (1991) Enemy recognition and defence within trophobiotic associations with ants by the soldier caste of Pseudoregma sundanica (Homoptera: Aphidoidea). Entomol Gener 16:1–12 Setzer RW (1980) Intergall migration in the aphid genus Pemphigus. Ann Entomol Soc Am 73:327–331 Shibao H (1998) Social structure and the defensive role of soldiers in a eusocial bamboo aphid, Pseudoregma bambucicola (Homoptera: Aphididae): a test of the defence-optimization hypothesis. Res Popul Ecol 40:325–333 Shibao H (1999a) Reproductive schedule and factors affecting soldier production in the eusocial bamboo aphid, Pseudoregma bambucicola (Homoptera: Aphididae). Insectes Soc 46:378–386 Shibao H (1999b) Lack of kin discrimination in the eusocial aphid Pseudoregma bambucicola (Homoptera: Aphididae). J Ethol 17:17–24 Shibao H, Kutsukake M, Lee J-M, Fukatsu T (2002) Maintenance of soldier-producing aphids on an artificial diet. J Insect Physiol 48:495–505 Shibao H, Lee J, Kutsukake M, Fukatsu T (2003) Aphid soldier differentiation: density acts on both embryos and newborn nymphs. Naturwissenschaften 90:501–504 Shibao H, Kutsukake M, Fukatsu T (2004a) Density triggers soldier production in a social aphid. Proc R Soc Lond B (Suppl) 271:S71–S74

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Shibao H, Kutsukake M, Fukatsu T (2004b) Density-dependent induction and suppression of soldier differentiation in an aphid social system. J Insect Physiol 50:995–1000 Shingleton AW, Foster WA (2000) Ant-tending influences soldier production in a social aphid. Proc R Soc Lond B 267:1863–1868 Shingleton AW, Foster WA (2001) Behaviour, morphology and the division of labour in two soldierproducing aphids. Anim Behav 62:671–679 Stern DL (1998) Phylogeny of the tribe Cerataphidini (Homoptera) and the evolution of the horned soldier aphids. Evolution 52:155–165 Stern DL, Foster WA (1996) The evolution of soldiers in aphids. Biol Rev Camb Philos Soc 71:27–79 Stern DL, Foster WA (1997) The evolution of sociality in aphids: a clone’s-eye view. In: Choe JC, Crespi BJ (eds) Social behaviour in insects and arachnids. Cambridge University Press, Cambridge, pp 150–165 Stern DL, Aoki S, Kurosu U (1994) A test of geometric hypotheses for soldier investment patterns in the gall producing tropical aphid Cerataphis fransseni (Homoptera, Hormaphididae). Insectes Soc 41:457–460 Sunose T, Tsuda K, Ohseko S (1982) Seasonal change in ratios of soldier in a population of the bamboo aphid, Psuedoregma bambucicola. Bull Soc Popul Ecol 35:59–61 Tyerman JB, Roitberg BD (2004) Factors affecting soldier allocation in clonal aphids: a life-history model and test. Behav Ecol 15:94–101 Withgott JH, Abbot DK, Moran NA (1997) Maternal death relaxes developmental inhibition in nymphal aphid defenders. Proc R Soc Lond B 264:1197–1202

Chapter 3

The Evolutionary Ecology of Eusociality in Australian Gall Thrips: a ‘Model Clades’ Approach Thomas W. Chapman(* ü ), Bernard J. Crespi, and Scott P. Perry

Abstract We integrate phylogenetic information with data on genetic relatedness, inbreeding, sex ratios, reproductive skew, host-plant use, gall morphology, soldier defensive behavior, kleptoparasite pressure, and demography to evaluate hypotheses for the origin and evolution of soldier castes in Australian gall thrips. Necessary and sufficient conditions for the single origin of thrips soldiers appear to include high relatedness and inbreeding, strong kleptoparasite pressure, small brood size, and long duration of the gall. However, only brood size and gall duration apparently changed (becoming smaller) concomitant to the origin of soldiers. Reproductive skew between the foundress and soldiers was relatively low at the origin of soldiers, but increased substantially along the lineage leading to two species, Kladothrips habrus and K. intermedius, that also exhibit a relatively high propensity for defense by soldiers. Analysis of the associations between genetic and ecological traits that resulted from the social-adaptive radiation of gall thrips with soldiers indicated that (1) fewer matings by foundresses, and less mating after dispersal, result in stronger local mate competition, higher relatedness (and a higher inbreeding coefficient) among soldier females, and a stronger female bias in dispersers, and (2) gall size apparently constrains the reproduction of soldiers, with less soldier reproduction favoring the evolution of more-effective, more-altruistic soldiers; moreover, when soldiers are more effective, fewer of them need be produced, leading to higher production of dispersers. Soldiers were apparently lost in two lineages, in both cases in conjunction with a shift to a phylogenetically divergent species of Acacia host plant. Our analyses demonstrate that the evolution of soldiers in thrips is driven by a combination of selective pressures at three levels: from host-plant, to conspecific interactions, to kleptoparasites.

Thomas W. Chapman Department of Biology, Memorial University, St. John’s, NF A1B 3X9 Canada [email protected]

J. Korb and J. Heinze (eds.), Ecology of Social Evolution. © Springer-Verlag Berlin Heidelberg 2008

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Introduction

The evolution of eusociality is one of the classic problems in evolutionary biology, yet it has seldom been addressed in an explicitly phylogenetic context (see Chap. 2 on aphids and Chap. 10 on mole-rats). To analyze the evolution of social behavior, data on the diverse genetic, phenotypic and ecological causes of social system variation should be analyzed via inferences on a species-level phylogenetic tree. For most social insects, the origins of eusociality are so deep in antiquity that such studies are difficult or impossible (Hölldobler and Wilson 1990; Thorne 1997; Danforth 2002). However, some groups, such as the gall-inducing Acacia thrips, appear sufficiently young that robust inferences can be made regarding how their social systems have been assembled by selection (Crespi et al. 1998; Morris et al. 2001; Crespi et al. 2004). Australian gall-inducing thrips, Kladothrips, are small insects that produce a domicile in developing phyllodes (petioles modified to serve as both stem and leaf) on Acacia trees. Gall induction is linked to the availability of new phyllode growth stimulated by episodic rainfall in arid regions, and galls are only initiated on very young phyllode tissue (Mound 1971, 1994; Mound et al. 1996). A single female, called a foundress, in some species accompanied by a male, initiates the gall, and once completely interred she begins laying eggs (Crespi and Mound 1997). For 7 of the 23 described species of Australian gall-inducing thrips, the first individuals of the foundress’ brood to eclose are gall-bound soldiers, which are morphologically and behaviorally specialized for defending the fully winged dispersing brood (Crespi 1992a, 1992b; Perry et al. 2004). The galls formed by social thrips have been described as a ‘factory fortress’ since they provide both food and shelter for all occupants in a harsh, xeric environment (Crespi 1994; Queller and Strassmann 1998; Chapman et al. 2002; also see Chap. 2 on aphids). The concentration of these critical resources in a well-defined physical structure, and the limitation of gall induction to a short temporal window, means that there is extremely strong selection to defend or hide this resource against usurpers. Thrips species in the genus Koptothrips are specialist invaders of these galls that kill the occupants and then breed within the gall. Koptothrips are thought to be a major selective force underlying the evolution of soldier morphology and behavior (Crespi 1996; Crespi and Mound 1997; Crespi and Abbot 1999). Here, we review the evolutionary ecology of soldiers in thrips with a focus on the integration of phylogenetic information with data on genetics, phenotype, ecology, and demography. We describe a new approach to such an integration based on the concept of ‘model clades’: monophyletic groups for which sufficient multidisciplinary data are available to infer and evaluate scenarios for the joint roles of intrinsic and extrinsic factors in social evolution. First, we explain this approach, and how it extends previous approaches for comparative analysis. Second, we present our current hypothesis of phylogenetic relationships among gall thrips species with and without soldiers. Third, we describe how patterns of interspecific variation in genetic relatedness, inbreeding, sex ratios, reproductive skew, host-plant use, gall size and shape, kleptoparasite pressure, and soldier behavior have evolved, in our phylogenetic

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context. Fourth, we integrate these patterns and propose a scenario for the interplay of intrinsic and extrinsic forces in the origin and diversification of soldiers in Australian gall thrips. Finally, we describe salient convergences and divergences between these thrips and other social animals to further the development of general theory for how and why social behavior evolves.

3.2

A Model Clades Approach to Analyzing Social Evolution

Most analyses of the evolution of sociality have focused on inferring the adaptive significance of social behavior and social systems from functional-design studies on extant species. This approach has been especially fruitful using ‘model systems’ (Dugatkin 2001) such as the Hymenoptera Polistes fuscatus, Apis mellifera, Lasioglossum zephyrum and the aphid Pemphigus spyrothecae (see Chap. 2 on aphids) for which extensive studies have been performed on aspects of behavior, ecology, and molecular genetics. Packer (1991) pioneered the use of phylogenies for the study of social evolution, whereby the numbers and patterns of origins and losses of eusociality are reconstructed for an entire clade. This approach has since been applied to diverse social taxa (Stern and Foster 1996, 1997; Danforth 2002; Crespi et al. 1997; Choe and Crespi 1997) and extended by mapping data on one or few phenotypic traits relevant to social evolution onto the phylogeny, and linking inferred social-evolutionary trajectories to their putative causes (e.g., Ross and Carpenter 1991; Faulkes et al. 1997; Hunt 1999; Chapman et al. 2002). In this review, we integrate the phylogenetic approach to social behavior studies with the concept of ‘model systems’, by jointly analyzing diverse sources of data in the context of a species-level phylogeny for Australian gall thrips on Acacia. The rationale for this methodology is that origins, losses, and other transformations in social systems take place over evolutionary time scales, and are driven by changes in myriad ecological, demographic, morphological, and population-genetic traits. Thus, robust inference of the causes of social evolution over long-term time scales requires that multidisciplinary data be collected for an entire clade of social species and non-social relatives. Application of this ‘model clades’ approach is difficult because it requires a robust, more-or-less complete species-level phylogeny, combined with salient data on enough of the species for reasonable inferential and statistical power. However, such data, analyzed using ancestor-reconstruction and correlated-evolution methods (Felsenstein 1985; Harvey and Pagel 1991; Maddison and Maddison 1992; Pagel 1994; Doughty 1996), should yield a more comprehensive picture of the causes and patterns of evolutionary change in social traits than singlespecies studies or comparative analyses using small sets of paired variables. Here, we apply this model clades approach to deciphering the causes of the origin and diversification of sociality in Australian gall thrips by presenting the phylogenetic hypothesis for this group, inferring the ancestral traits of Australian gall thrips that are presumed to affect social evolution, and comparing across and within lineages without and with soldiers for socially relevant traits.

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Phylogeny

A well-resolved and well-supported phylogeny for Australian gall thrips on Acacia has been inferred using DNA sequence from the genes elongation factor 1a, wingless, cytochrome oxidase I, and 16S ribosomal DNA (Morris et al. 2001; Crespi et al. 2004). This phylogeny includes all of the described species except one (Kladothrips carneorum), and it exhibits strong bootstrap support for the monophyly of the group as a whole, and for most of the nodes. The sister-group to these gall-inducers (Dactylothrips and Rhopalothripoides) also lives on Acacia, but they are not gallinducing. Instead, they live in various enclosed spaces, such as old galls of other insects, or cracks in bark or stems. Some of these ‘opportunistic’ species exhibit wing polymorphism and some Dactylothrips show forms of parental care involving defense of their domicile using tergites modified into pincers (Crespi and Mound 1997; Crespi et al. 2004). Gall-induction apparently evolved from deformation of plant material (here, phyllodes) during feeding, as in other insect groups (Shorthouse and Rohfritsch 1992; Williams 1994; Crespi et al. 1997). The basal lineages of gall thrips, comprising K. pilbara, K. schwarzi, K. antennatus, and K. zygus, all inhabit Acacia in the highly arid zone. They induce simple tubular galls resembling tightly rolled phyllodes on Acacia species in the taxonomic sections Juliflorae and Phyllodineae, and adult offspring of the foundress eclose within the galls. The three, more-derived lineages can usefully be divided into three groups based on their host-plant relationships and life histories (Fig. 3.1). Lineage A is found on Acacia in the taxonomic section Juliflorae, also in the highly arid zone, where they induce more or less spherical and tightly closed galls that appear nearly impervious to invasion by natural enemies such as kleptoparasites; we thus refer to these species as ‘hiders’. All but one species in lineages B and C inhabit Acacia in the section Plurinerves, mostly in semi-arid regions. The species in lineage B induce relatively large galls of diverse forms that persist for relatively short lengths of time on the host plant, and they exhibit high fecundity relative to most of the species in lineage C (Table 3.1). With the possible exception of K. maslini, these species are heavily beset by kleptoparasites in the genus Koptothrips, as well as other natural enemies (Crespi and Abbot 1999); we refer to them as ‘fliers’, since their brief within-gall phase of the life cycle appears to be an adaptation to reduce vulnerability to these enemies. Lineage C, the ‘fighters’, includes all of the species with soldiers, plus two species without soldiers, K. xiphius and K. rodwayi. These species tend to exhibit a relatively small gall, which is associated with low fecundity, and the galls persist for a long time on the host plant (up to 1 year). There are two equally parsimonious inferences for the pattern and number of origins and losses of soldiers: (1) one origin at the base of the lineage, and two losses, one each in K. xiphius and K. rodwayi, vs. (2) two origins (one in K. hamiltoni + K. harpophyllae and one in K. morrisi + K. waterhousei + K. habrus + K. intermedius + K. rodwayi), followed by one loss (in K. rodwayi) (Morris et al. 2001). Two lines of evidence support the former scenario of one origin. First, the hypothesis that the lineages leading to both K. xiphius and

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Fig. 3.1 Phylogeny for species of gall-inducing thrips on Acacia, from Morris et al. (2001) and Crespi et al. (2004). Numbers beside the branches are bootstrap support values from maximum parsimony analysis/maximum likelihood analysis (1,000 and 100 replicates, respectively), with only one value shown when it was the same in both analyses. Species of Dactylothrips and Rhopalothripoides were used to root the tree (Morris et al. 2001; Crespi et al. 2004). Acacia host plant species from which the thrips were sampled are shown in parentheses. The analysis is based on COI, 16S, and microsatellite data, and K. rugosus, K. waterhousei, K. augonsaxxos, and K. schwarzi each represents a suite of 6–15 sibling species or host-plant races (Crespi et al. 1998, 2004). Circled letters indicate ancestral lineages that have lead to the extant taxa exhibiting one of three defensive strategies: A ‘hiders’; B ‘fliers’; C ‘fighters’. Species with soldiers are in bold. Kladothrips sterni has a within-gall morph that does not function as a soldier

375 460 433 313

338/139

403/128 –/266 –/132 –/286 –/30

Data are from Crespi et al. (2004)

37

Gall volume

172/58

Number of dispersers

79

Solitary species

7

K. rodwayi K. xiphius K. rugosus (Ac. papyrocarpa) K. ellobus K. arotrum K. antennatus K. acaciae K. schwarzi

K. waterhousei 50/16 (Ac. papyrocarpa)

1020/337

K. morrisi

619

60

15 38

115

25

246/89 –/65 136/54

105

10

135/31

K. habrus (Ac. melvillei) K. hamiltoni K. harpophyllae K. intermedius

9

25

21

52

16

41 6 5

51

12

Disperser % male

47

41

15

6

51

0.60

0.73 0.21

0.54 0.52

0.67 0.09–0.59

–0.13

0.45 0.02

0.31

0.34

0.30 0.63 1.0 0.31

0.70

0.31

Female Foundress disperser inbreeding relatedness level Fis

0.83 1.0 no sex dif- 0.72 ference no sex dif- 0.62 ference females 0.65 first

females first males first

0.35

0.45

0.07

0.38

0.16

Table 3.1 Behavioral, ecological, population-genetic, and life history traits of gall-inducing thrips on Australian Acacia Gall volume Number Number Soldier Female Foundress Soldier (mm3) of of Soldier Disperser eclosion by soldier inbreeding inbreeding Skew, Social species total/inner soldiers dispersers % male % male sex relatedness level Fis level Fis msat

0

0

6 50 0

0

40 0 2 35

7

0

45 0 0

0 0 42

% galls % with male Koptothrips founder

32

29

25 25 31

23

% galls % with male Koptothrips founder

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K. rodwayi evolved via loss of soldiers is consistent with their habitation of Acacia host plants that are phylogenetically highly divergent from the Acacia inhabited by the other thrips species in this clade (Crespi et al. 2004). Indeed, such large-scale host plant shifts are apparently always associated with substantial phenotypic and life-historical changes in Australian gall-inducing and related thrips on Acacia (Crespi et al. 2004). Second, Wcislo and Danforth (1997) present evidence that ancient origins, punctuated by scattered losses, characterize the evolution of eusociality in other insect groups; this pattern may be related to the complex nature of the trait ‘eusociality’, which by Dollo’s ‘law’ would make it evolutionarily difficult to gain (via multiple steps) but easy to lose (via a change in any of a large suite of traits, at least for so-called primitively eusocial forms) (see also Danforth 2002). The hypotheses of one vs. two origins of soldiers can best be tested further via testing for homology, parallelism or convergence in the genetic or physiological underpinnings of soldier morphs. At present, we provisionally accept the single-origins hypothesis and note that our inferences about character change are not qualitatively altered if the hypothesis is later rejected.

3.4 3.4.1

Variation in Traits Related to Sociality The groundplan of Australian Gall-Inducing Acacia thrips

Three traits of the insect order Thysanoptera are especially relevant to the origin and evolution of soldiers. First, all thrips are haplodiploid (Stannard 1968; Crespi 1991, 1993; Mound and Heming 1991). As in Hymenoptera, this genetic system engenders sex-ratio manipulation by mothers, reproduction by virgins, the potential for relatedness above 0.5 and relatedness asymmetries between the sexes, and a genetic tolerance to inbreeding (Chapman 2003). Second, as in aphids (see Chap. 2 on aphids), the forelegs of thrips can be readily modified to serve as weaponry, as evidenced by the high frequency of male foreleg allometry and male fighting within this order (Crespi 1986, 1988, 1993). Moreover, intraspecific fighting is common in thrips (as in some aphids), and it provides the raw material for selection on interspecific defense against natural enemies (Whitham 1979; Aoki and Makino 1982; Crespi et al. 1997; Crespi and Mound 1997; Inbar 1998). Third, as in aphids, ants, and termites, wing polymorphism is common in Thysanoptera (and in Acacia thrips related to those that induce galls on this plant genus). Wing polymorphism can serve as a template for the evolution of soldiers, as the evolutionarily facile reduction or loss of wings can free up physiological resources (Roff 1986; Roff and Fairbairn 1991; Roff and Bradford 1996) for the development of weaponry such as enlarged forelegs, as well as for reproduction. Indeed, in K. intermedius (formerly called Oncothrips tepperi), soldiers show a strong negative correlation between wing length and foreleg size (Crespi 1992a). The evolution of soldiers only in the thrips that induce galls on Australian Acacia can, we believe, be traced to the unique nature of the gall as a resource, and the harsh

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environment of the Australian interior (see Chap. 7 on termites and Chap. 2 on aphids for additional discussion of impacts of the coincidence of food and shelter). Thus, Acacia galls can only be induced during the very short temporal window when new phyllodes are being produced by the host plant, annually in many species and less frequently in areas of more-unpredictable rainfall. A gall represents food, shelter and reproduction for a lifetime, it cannot be replaced if lost, and the environment outside of the gall is among the most harsh and arid on earth. The high value of galls, and the ecological constraints associated with their induction, makes them a coveted resource for natural enemies, and soldier morphs represent one adaptive life-history strategy (in addition to a short life cycle, or a tightly enclosed gall) for maximizing inclusive fitness in the face of such strong selection.

3.4.2

The Origin of Soldiers

Given that Thysanoptera in general, and Australian gall thrips in particular, exhibit several crucial preadaptations to the evolution of soldiers, we are next faced with the question of why soldiers originated in one particular lineage and why they were lost in others. Addressing these questions requires inferring the states of diverse ecological, morphological, demographic, genetic, and other traits at the branch subtending the origin of eusociality, as well as inference of which of these traits changed along this branch, and how. Figure 3.2 shows that the lineage leading to the origin of soldiers apparently exhibited a suite of traits that remained more or less constant during the transition, but apparently formed important parts of the selective context whereby soldiers evolved. These traits include: (1) fighting in foundresses, (2) a male founder being present in a substantial proportion of galls, (3) high relatedness among gall-mates, and substantial inbreeding in the foundress, and (4) attack by Koptothrips kleptoparasites, and (5) pupation of dispersers in the soil. Thus, the context for the origin of soldiers involved the morphology and behavior of foundresses in defending against Koptothrips serving as an apparent pre-adaptation to within-gall defense by offspring. Moreover, inclusive fitness effects can be inferred to have been strong, as soldiers of both sexes were closely related to siblings and their mother, due to inbreeding, a lack of inter-gall mixing at any stage, and the presence of a male founder leading to broods being comprised of full siblings. Finally, the inferred presence of attack by Koptothrips during the transition to soldiers is consistent with the hypothesis that they represent one of the main selective forces for soldier evolution (in conjunction with intra-gall reproduction by offspring), but also that Koptothrips attack did not coincide with and precipitate the origin of soldiers. Three species in the sister-group to the lineage with soldiers, K. rugosus, K. ellobus, and K. acaciae, and the social species K. harpophyllae, exhibit a substantial incidence (on the order of 50% of galls) of single male founders being present at gall initiation, a pattern evidently driven by male fighting and mate guarding (Crespi 1992b). This mating system might also lead to split sex ratios, if some foundresses

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Fig. 3.2 Scenario for the evolution of social behavior in Australian gall thrips, based on our ‘model clades’ approach. The origin, diversification, and loss of soldier castes is driven by a combination of genetic, physiological, morphological, ecological, demographic, and behavioral traits, evolving together. Lineages shown in black have soldiers; grey lineages indicate an absence of soldiers. The ancestral population of the gall thrips is thought to have large broods produced by a single physogastric female who has likely mated with a brother before gall initiation; consequently there is high relatedness (r) within these galls. Foundresses in this ancestral population are likely to have fought for gall initiation sites; a pre-adaptation to soldiering. These ancestral broods would pupate within the gall. There has been a host-plant shift inferred to the Plurinerves at the point marked ‘1’ on our phylogeny. At this point, male founders are thought to accompany females, Koptothrips parasitism arose, and brood leaves the gall to pupate in the soil. At point ‘2’ is thought to be the origin of soldiers, a loss of physogastry and consequently smaller brood sizes, a correlated reduction in gall volume and an elongation of gall shape; along with a longer gall duration. At point ‘3’ there is a loss of male founders. At point ‘4’ soldier reproductive output is reduced with a correlated increase in soldier efficiency. The lineage leading to K. intermedius has reverted to brood pupation within the gall. Host shifting events (between Acacia species) are indicated with the illustration of trees and an arrow. This symbol is placed above the lineage where the shift is thought to have occurred

inbreed before dispersal while others mate after dispersal with a non-relative. Galls with male founders should thus exhibit single mating by foundresses with an unrelated male, and high relatedness of brood within galls. Similarly, K. rugosus, a species in the sister clade to the clade bearing soldiers, exhibits ‘split’ sex ratios due to a notable incidence of foundress virginity (Kranz et al. 2000). Both of these split sexratio effects could have disproportionately favored the origin of soldiers in some subset of galls, where Hamilton’s rule was satisfied (Grafen 1986; Godfray and

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Grafen 1988); this hypothesis can be tested further via studies of K. harpophyllae, the only species with soldiers and a high incidence of male founders. The lineage giving rise to soldiers apparently exhibited large galls with many dispersers and soldiers relative to more-derived lineages, relatively high reproduction by soldiers (Chapman et al. 2002), relatively high FIS values for foundresses, among-soldier relatedness that was high but not notably so, and a relative male bias to the sex ratio of soldiers; the sex ratio of dispersers is difficult to infer with any confidence, as it differs so strikingly between K. morrisi (41%) and K. hamiltoni (6%). These inferences can be interpreted in the context of the inclusive fitness model of Chapman (2003), which elucidates the expected role of sex ratios, inbreeding and soldier reproduction in the origin of helping by male and female proto-soldiers. This model predicts two main patterns that accord with the inferences from phylogenetics and character mapping. First, based on considerations of relatedness and inbreeding, the model predicts a lower soldiering threshold in males than females, which fits with the relatively high proportion of male soldiers in K. hamiltoni (52%) and K. morrisi (25%) compared to the other species, assuming that there are factors other than relatedness and inbreeding (such as sex differences in body size) that affect this trait. Second, the model demonstrates that reproduction by male and female proto-soldiers favors the origin of helping, by raising the FIS of dispersers and leading to alternating FIS between generations, which can make soldiers more highly related to natal colony mates than they would be to their own offspring. This effect represents an interesting combination of Trivers and Hare’s (1976) hypothesis that female proto-helper reproduction should have favored the origin of hymenopteran eusociality, and Bartz’s (1979) ideas on the potential role of inbreeding/ outbreeding cycles in termites. In general, the presence of bisexual helping in social thrips can also be attributed to the high similarity in morphology of female and male Acacia gall thrips, with both sexes similarly armed (though females tend to be larger in overall size), and the tendency of strong inbreeding to reduce the relatedness asymmetries of haplodiploidy (Chapman and Crespi 1998). However, the presence of soldiers of both sexes may belie important sex differences in willingness to defend (i.e., who takes on the risky task of attacking a Koptothrips first) (Crespi and Mound 1997). Coinciding with the inferred origin of soldiers were changes in four traits: (1) galls became smaller and evolved from being relatively round to flat or elongate, (2) foundresses became non-physogastric, (3) broods evolved to be smaller, and (4) galls persisted for considerably longer on the host plants (time for soldiers to eclose) (Crespi et al. 1997; Crespi and Worobey 1998; Kranz et al. 2001a, 2001b; Crespi et al. 2004). These four traits are closely related and presumably evolved in concert. Small galls are strongly associated with small broods because gall volume imposes constraints on brood size, and small broods are associated with a lack of physogastry. Given that most of the species with soldiers utilize host plants that are also occupied by congeneric gall thrips with larger, rounded galls and without soldiers (Crespi et al. 1997, 2004), gall size cannot be intrinsically constrained by phyllode size. Instead, we propose that large-gall and small-gall species have evolved to utilize the gall resource either quickly, leading to a short life cycle, or slowly, leading to the

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prolonged life cycle of species with soldiers. These findings also suggest that species with soldiers have lower within-gall population growth rates, which theoretical models predict should favor the evolution of soldier defense in the ecologically similar gall aphids (Akimoto 1996; Stern and Foster 1996; Chap. 2 on aphids). High colony longevity, which is also found in aphid species with soldiers (Moran 1993; Foster and Northcott 1994; Rhoden and Foster 2002), may have favored the origin of soldiers because galls are thereby vulnerable to natural enemies for longer periods. Longevity might also be a consequence of soldiers, whose presence could allow galls to persist longer in relative safety; however, species with soldiers do not exhibit lower rates of successful Koptothrips parasitism, apparently because Koptothrips often invade before soldiers eclose, and defense by soldiers is only partially effective (Crespi and Abbot 1999; Chapman et al. 2006). A pattern of high parasite pressure favoring the origin and maintenance of sociality has also been proposed for some Hymenoptera (Lin 1964; Lin and Michener 1972; Kukuk et al. 1989), and other social taxa (Crespi and Choe 1997). Species with soldiers also tend to induce relatively flat or elongate galls, which, coupled with their small size, generates a relatively high inner surface area-to-volume ratio. Such gall morphologies are presumably related to the space available for feeding inside, relative to the number of inhabitants. High inner gall surface area to volume ratio is also found in the galls of two gall thrips that are unrelated to the species with soldiers and their sister-group: Kladothrips sterni on Acacia aneura, and Iotatubothrips crozieri on Casuarina, both of which undergo multiple generations in the gall. A clear relationship between multiple generations and high inner gall surface area has thus evolved convergently at least three times (Crespi and Worobey 1998), which suggests that space for feeding is related in some way to gall lifespan. Indeed, these patterns suggest strong causal connections between thrips demographics, life history, gall morphology and physiology, and soldiering. Stone and Schönrogge (2003) describe analogous adaptations of gall morphology to demography and defense, in diverse species of insects. Chapman et al. (2006) have also explored the possibility that elongate galls in the social species may have arisen in order to increase the speed with which the gall develops while minimizing the loss of inner surface area for feeding; a strategy that may have come about in response to kleptoparasitic invasion pressure focused on the period before soldier eclosion in the gall life history; that is, a more elongate gall may enclose the foundress more quickly enabling her to begin laying eggs sooner, thus soldier eclosion will also occur sooner. In these galls, relative to a more pouched gall, the window of opportunity for Koptothrips to invade before soldier development is reduced. Understanding the connections between gall morphology, demography, ecology and behavior requires further study, especially as it appears to involve low fecundity and enhanced adaption for defense from natural enemies. As an apparent exception that supports the rule, K. morrisi, one of the few gall thrips with soldiers that is the only gall-inducer on its host plant, exhibits a suite of life-history traits that combines elements of the soldiering species (i.e., soldiers and an elongate gall) and their significantly more fecund, solitary sister-lineage (i.e., large galls and large brood) (Kranz et al. 2001a).

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Diversification Among Species with Soldiers

How and why, in the lineages with soldiers, has diversity in socially salient traits such as relatedness, inbreeding, life cycle, sex ratios, reproductive skew, and soldier behavior evolved?

Relatedness and Inbreeding Along with his ¾ relatedness hypothesis, Hamilton (1964) suggested that it may also be necessary to invoke inbreeding to explain some phenomena observed in social insects, while Wilson (1975) went further in linking inbreeding and eusociality by stating that the effect of inbreeding on the evolution of social behavior is one of the central issues of sociobiology. Inbreeding has been shown theoretically to increase the likelihood of genes for social behavior spreading to fixation within a population (e.g., Michod 1993; Wade and Breden 1987; Breden and Wade 1991). Support for high levels of relatedness giving rise to sociality has been limited to high relatedness estimates in some primitively eusocial forms (Crozier et al. 1987; Ross and Carpenter 1991), the tendency for helping by females only in Hymenoptera (Hamilton 1964), and a large number of origins of eusociality in the Hymenoptera (Hamilton 1964; Andersson 1984; Alexander et al. 1991). Evidence against haplodiploidy playing a notable role in social evolution is the observations of social behavior in diploid species (e.g., termites), and the frequent observation in haplodiploid social colonies of multiple mating and multiple queens (see Chap. 6 on ants), which can lower the relatedness of females in a colony to below 0.5. These observations of extant social species provide strong evidence that unusually elevated levels of within colony relatedness are not necessary for the maintenance of sociality and question the importance of haplodiploid-relatedness-asymmetries in the origin of social behavior. Similarly, there is little evidence that inbreeding plays an important role in the origin or maintenance of sociality, as inbreeding has only been documented in a limited, although diverse, number of social species, including naked mole rats (Reeve et al. 1990; see Chap. 10 on mole-rats), social thrips (Chapman and Crespi 1998; Chapman et al. 2000), social spiders (Avilés 1997), and some termites (see Chap. 7 on termites). However, with regard to the origin of eusociality, an explicitly historical or phylogenetic analysis of inbreeding and relatedness has only been undertaken in the social thrips. Population-genetic (microsatellite) data have shown that inbreeding is common in the gall-inducing thrips on Acacia both with and without soldiers, however, its strength diverges considerably among these species (Chapman and Crespi 1998; Chapman et al. 2000; McLeish et al. 2006; Table 3.1). Elevated levels of relatedness have also been detected in many social species (Chapman and Crespi 1998; Chapman et al. 2000). These estimates of inbreeding and relatedness mapped onto the phylogeny of the gall-inducers have led to the inference of unusually high relatedness, due in part to high levels of inbreeding, near to the origin of soldiers, and

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that high levels of inbreeding emerged well before the evolution of a sub-fertile caste (Fig. 3.2). Character optimization indicates that the ancestral population that gave rise to soldiers may have had an average relatedness among soldiers, males and females taken together, of 0.78 and an inbreeding coefficient of 0.58 (single origin of soldiers hypothesis, Chapman et al. 2000), and subsequently, these values evolved to be lower in more-derived social lineages. An ancestral population with such high levels of inbreeding would have greatly reduced relatedness asymmetries, which are central to Hamilton’s 3/4 relatedness hypothesis. These findings cast doubt on the importance of haplodiploid relatedness asymmetries on thrips social evolution. However, the gall-forming thrips do provide the most concrete example of an inbreeding population giving rise to social lineages, and, as discussed below, inbreeding has apparently impacted the origin and forms of social behavior.

Soldier Reproduction and Gall Morphology Crespi (1992a) reported the first evidence that the wing-reduced individuals in thrips induced Acacia galls were defensive specialists. Crespi (1992a) also determined through dissections that these defensive specialists were sexually mature and perhaps capable of reproducing within the gall, but he surmised that their reproductive output was likely to be limited by available space within the gall. Chapman et al. (2002) largely confirmed this assertion by estimating the degree of reproductive differentiation between foundresses and soldiers in multiple populations of five species of gall-inducing thrips using microsatellite data and ovarian dissections. Microsatellite-based species estimates of average per capita reproductive output of soldiers relative to the foundresses ranged from 0.005 to 0.64. Estimates were based on one or two microsatellite loci only. The paucity of polymorphic loci, likely due to population bottlenecks from frequent bush-fires and droughts in the Australian outback, and the large amount of inbreeding present in many of these species meant that conventional maternal analysis using co-dominant markers was not possible. Instead, estimates were obtained by assessing the difference in inbreeding coefficients as measured in soldiers and in dispersers. A mathematical relationship was developed that allowed the inference of soldier reproduction from the expected increase in the inbreeding coefficient, as measured in the dispersers, which was likely due to soldier production of female dispersing offspring. Males are not useful for estimating observed homozygosity levels and consequently were not taken into account in these estimates. Therefore, an underestimation of soldier reproductive output is expected if soldiers produce a greater proportion of males compared to that of the foundress. Soldier breeding has been shown theoretically to alter the probability of genes in colony founders being transmitted to the dispersing generation through male and female soldiers (the ‘reproductive value’ of males and females) from that expected for a haplo-diploid colony with no reproduction by helpers (Chapman 2003). This proposed change in reproductive value of male and female offspring leads to the expectation that female soldiers would produce a

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less female biased sex ratio compared to their foundress mothers. The second method utilized here, ovarian dissections, is not impacted by the sex ratio produced but simply indicates the potential for egg laying between soldiers and her foundress mother. These estimates, based on ovarian dissections, ranged from 0.17 to 1.1. Given that these potential eggs may not all translate into actual offspring produced, these estimates may represent overestimations of soldier reproduction. However, both approaches reveal similar variation in reproduction by the soldier group across species, and there is a strong, significant correlation between the microsatellite and ovarian-dissection estimates (Chapman et al. 2002). The mapping of the microsatellite-based and ovarian-dissection-based estimates of relative soldier reproduction showed the same phylogenetic pattern, that levels of soldier reproduction were apparently higher in three more-basal lineages than in the two most derived lineages (Chapman et al. 2002). The inference is that thrips soldier morphology and behavior likely evolved in the presence of considerable levels of soldier reproduction. This scenario is consistent with philopatric offspring developing traits such as enlarged forelimbs and evolving into defensive specialists that only later evolved lowered fecundity. Correlated with this lowered reproductive output by soldiers was a shrinking of the average volume of a gall (r2 = 0.89, p< 0.05, using independent contrasts, Wills et al. 2004). These observations are consistent with gall volume constraining the reproductive output of soldiers, as Crespi (1992a) anticipated. The progenitor of the modern thrips soldier appears likely to have been a nondispersing morph that reproduced via sib-mating within its natal gall. With the subsequent loss of some direct reproductive output, the evolutionary maintenance of the developing soldier caste provides somewhat of a conundrum. The impact of the reproductive output of a proto-soldier on soldier evolution was investigated using an inclusive fitness model (Chapman 2003). Parameters in the model included mixed mating, a female biased sex ratio, and proto-soldier reproduction and the impact of these parameters on the relatedness between the potential soldier and its gall mates. In general, the results of the model indicated that allowing for some proto-soldier reproduction increased the likelihood of the evolution of a soldier caste for both female and male proto-soldiers. The main impact was that proto-soldier reproduction increased the inbreeding coefficient of the disperser generation over that of the proto-soldiers, resulting in alternating levels of inbreeding between generations. This oscillation in inbreeding coefficients favors soldiers by increasing the relatedness of a proto-soldier to natal colony mates relative to the relatedness it would have to its own offspring. However, the amplitude and the predicted impact of these oscillations on the evolution of soldiering are reduced as sib-mating increases within the dispersing generation. Thus, a high level of inbreeding by the foundress reduces the difference in the inbreeding coefficients between the dispersers and proto-soldiers and reduces relatedness differences for helping versus reproducing. High inbreeding and high levels of female soldier reproduction at the origin of soldiers, and the subsequent reduction of both traits in the two most derived species of gall-inducers, are consistent with the model in that inbreeding by foundresses may retard the evolution of extreme levels of altruism.

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For male proto-soldiers, inbreeding by the foundress and proto-soldier reproduction both act to decrease the helping threshold. That is, when inbreeding by dispersers is high and proto-soldiers produce some of the dispersing generation, male protosoldiers are more likely to find themselves in a position where an altruistic act within their natal nest may have a greater inclusive fitness payoff than the pursuit of direct fitness alone. As discussed below, the effects of inbreeding on male and female helping thresholds have important implications for the evolution of soldier sex ratios.

Soldier Defensive Ability In Acacia gall thrips, the transition from a solitary to social life history also included a reduction in gall volume and a consequent reduction in disperser numbers, as well as an elongated period for the development of dispersing brood (Wills et al. 2001, 2004; Crespi et al. 2004). Thus, gall-inducing thrips lineages have evolved to adopt either of two strategies under selective pressure from Koptothrips invasions: (1) produce large galls and fast developing brood in order to ameliorate losses due to Koptothrips invaders, or (2) produce small galls, and therefore smaller dispersing brood numbers, but increase the survival of these galls by producing a specialized defending caste (the soldiers) (Crespi et al. 2004). The second strategy, defense of galls by soldiers, involves a trade-off between the number of dispersers produced and survival of the gall until dispersal. The soldiers themselves appear to make an additional trade-off. Thus, the reproductive output of thrips soldiers ranges widely (Chapman et al. 2002), and soldier defensive efficacy appears to be negatively correlated with the degree to which soldiers reproduce (r = −0.88, P = 0.0489, N = 5 by simple correlation; r= − 0.84, P = 0.076 using independent contrasts, Perry et al. 2002, 2004). Given evidence for a relationship between soldier reproduction and defensive ability, the mechanism and source of the trade-off remain unclear. Crespi (1992a) showed that in one species, Oncothrips tepperi (now K. intermedius), soldiers exhibit an inverse relationship between wing length and foreleg (weaponry) size, which is consistent with a developmental trade-off between defense and dispersal. Such a trade-off could have helped to favor the origin of thrips soldiers by making within the gall philopatry more beneficial energetically; in other insects, reduced wings tend to be associated with increased fecundity (Roff 1986). However, the relationship of wing length and foreleg size with reproductive output in thrips is not yet known. Trade-offs between direct reproduction and benefits to kin via defense, such as the ones discussed here in Acacia gall thrips, have also been fundamental to the evolution of ‘advanced’ eusociality in Hymenoptera and Isoptera (Bourke and Franks 1995; Thorne 1997; Chapman et al. 2002). In thrips, further tests of the relationships between reproductive skew, soldier behavior, and other variables require the addition of data from more species to alleviate the low statistical power currently available (e.g., there are over 12 species in the K. waterhousei complex; Crespi et al. 2004), as well as comparative analyses that include additional variables, such as weapon morphology and degree of gonadal development

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Evolution of Sex Allocation, Ecology, Genetic Structure and Sociality Theories linking sex allocation with the origins and forms of eusociality have long held a central and controversial role in the debate over the causes of the evolution of social behavior (Hamilton 1972; Trivers and Hare 1976; Charnov 1978; Seger 1983; Grafen 1986; Godfray and Grafen 1988; Crozier and Pamilo 1996; Hardy 2002). Australian Acacia thrips are especially useful for addressing these links because thrips are the only taxon other than Hymenoptera exhibiting both eusociality and facultative sex-ratio manipulation via haplodiploidy. The main factors predicted to affect the evolution of Acacia gall thrips sex allocation include: (1) local competition between relatives within the gall, especially competition between males for mating with sisters leading to female-biased sex allocation; (2) levels of relatedness and inbreeding, which determine the ratio of male to female offspring that maximizes inclusive fitness of the female controlling allocation; these values are set by numbers of matings by females, the extent to which these matings take place before and after dispersal from the gall, and the extent to which soldiers reproduce; and (3) any conflict between foundresses and female soldiers over sex allocation ratios, which is analogous to queen-worker conflict over sex allocation in Hymenoptera (see Chap. 6 on ants). We can analyze these selective pressures using comparative data from five of the seven described species with soldiers on gall sizes, numbers of soldiers and dispersers, disperser sex ratios, soldier sex ratios, relatedness, inbreeding coefficients of foundresses and soldiers, levels of reproductive skew between foundresses and soldiers, soldier propensity to attack Koptothrips, and soldier efficacy in killing these enemies (Table 3.1). The variables show marked variation among these five species. The patterns of correlation between traits demonstrate that their causal connections fall into two main clusters: (a) effects of mating system and relatedness on sex allocation (Fig. 3.3), and (b) effects of ecology on sociality, which appear to be more or less independent of sex allocation (Fig. 3.4). Mating system effects on sex allocation can be inferred from the associations between disperser and soldier sex ratios, disperser and soldier inbreeding coefficients (FIS), and relatedness between female soldiers (Fig. 3.3). Three main patterns are evident: (1) higher relatedness between soldiers is strongly associated with more female-biased disperser sex ratios, (2) disperser and soldier FIS values are strongly and positively correlated, and (3) foundress and soldier FIS values are positively correlated with soldier sex ratio. A strong though non-significant positive correlation is also apparent between female soldier relatedness and soldier sex ratio, and soldier and disperser sex ratio appear to be negatively correlated across species. Taken together, these results suggest that fewer matings by foundresses, and less mating after dispersal, result in stronger local mate competition, higher relatedness (and a higher inbreeding coefficient) among soldier females, and a stronger female bias in dispersers. Indeed, in the two cases where there is an unbiased disperser sex ratio, inbreeding among dispersers has not been detected

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Fig. 3.3 Correlations between genetic and sex-ratio traits for the species of Australian gall thrips with soldiers. Species-level product-moment correlations are shown in boldface, and correlations based on phylogenetically independent contrasts are shown in plain text. Correlation coefficients with an asterisk (*) are significant at less than the 0.05 level

(O. waterhousei, Chapman et al. 2000) or multiple mating has been implicated in lowered relatedness (O. habrus, Chapman and Crespi 1998). Reproduction by soldiers varies considerably among species, and it complicates the expected relationships between inbreeding, relatedness and sex allocation. If female soldiers reproduce relatively little (as in K. habrus and K. intermedius), then soldiers and dispersers are genetically more or less equivalent, with an FIS determined by foundress mating patterns. By contrast, substantial reproduction by soldier females, which necessarily involves sibmating, raises the FIS of dispersers and creates inbreeding/outbreeding oscillations that may have favored the origin and evolution of helping (Chapman 2003); indeed, such oscillations appear to have been retained in K. hamiltoni and K. morrisi, the two most-basal species with soldiers (Table 3.1). In addition, the relative mating success of soldier and disperser males may differ; given partial bivoltinism (Seger 1983) soldier males may mate with both soldier females and disperser females, whereas disperser males eclose so late that they could only produce offspring via mating with disperser females.

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Fig. 3.4 Correlations between demographic, gall-morphological, reproductive, and behavioral traits, for the species of Australian gall thrips with soldiers. Species-level product-moment correlations are shown in boldface, and correlations based on phylogenetically independent contrasts are shown in plain text. Correlation coefficients with an asterisk (*) are significant at less than the 0.05 level. Skew refers to the per-capita reproduction of female soldiers compared to the foundress, which was estimated using microsatellite markers (msat) and ovarian dissections (demog)

Sex ratios vary among species, and they also exhibit a temporal variation, as one sex can be produced before the other. Among the social species studied in detail thus far, there are notable associations between the order of eclosion by sex in soldiers and three variables: soldier sex ratios, offspring sex ratios, and the extent of reproductive skew between female soldiers and foundresses (Kranz et al. 1999, 2000, 2001a, 2001b; Chapman et al. 2002). Thus, K. habrus and K. waterhousei exhibit protogynous (females first) soldier production, strongly female-biased soldier sex ratios, an unbiased sex ratio of reproductive dispersers, and relatively high skew. By contrast, K. hamiltoni exhibits the opposite pattern: protandrous (males first) soldier production, unbiased soldier sex ratio, a very strong female bias in dispersers, and

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relatively low skew. Moreover, K. morrisi and K. intermedius exhibit sex ratio patterns intermediate between these two extremes. These patterns suggest sex-ratio manipulation by foundresses is constraining the reproductive strategies of soldiers. Thus, protogyny, as found in K. habrus and K. waterhousei, forces soldier females to produce male reproductives because they are unmated. The foundress is favored by frequency-dependence to produce most or all of the female reproductives, resulting in higher skew and a relatively unbiased disperser sex ratio. By contrast, protandry may be favored to ensure that female soldiers can sib-mate soon after eclosion, under a breeding system with especially strong inbreeding (as in K. hamiltoni); in such a situation, a foundress can be more closely related to her granddaughters than her daughters (Kranz et al. 1999), which should also favor the evolution of relatively low reproductive skew. Protandrous production of soldiers may also engender higher motivation (and perhaps more developed defensive morphology) in male soldiers than female soldiers, since after male soldiers have mated their reproductive opportunities diminish and their main option for further maximizing inclusive fitness relies on alloparental defense. This prediction may help explain the unusual, unbiased soldier sex ratio found in K. hamiltoni. This is not true for female soldiers, who can continue to oviposit for as long as their offspring will have time to develop. Because production of dispersers is limited by gall size and not by the number of female soldiers, foundresses may be able to encourage defensive behavior in their sons by overproducing males. By contrast, protogynous soldier production should instead involve relatively high levels of investment in defense by female soldiers, in part because higher reproductive skew means that female soldiers gain relatively more in fitness from alloparental behavior. Preliminary data from K. habrus supports such a tendency for female soldiers to defend the gall more readily than male soldiers (Crespi and Mound 1997). Sex-ratio patterns in social thrips are intimately associated with relatedness and inbreeding, but they appear not to be directly related, in extant species, to ecological and social-behavioral traits such as gall size, colony size, levels of skew, and efficacy of soldiers in defense (Crespi et al. 2004). These variables are, however, closely related among themselves, with gall volume positively correlated with number of soldiers and number of dispersers, gall volume and number of soldiers each negatively correlated with soldier efficacy in gall defense, and reproductive skew (here, the amount of reproduction by soldiers compared to foundresses) positively correlated with gall size and number of dispersers, and negatively correlated with soldier efficacy. The most parsimonious explanation for these findings is that gall size constrains the reproduction of soldiers, less soldier reproduction favors the evolution of better, more altruistic soldiers, and when soldiers are better fewer of them need be produced, leading to higher production of dispersers. Further analysis of the causes of interspecific and temporal sex ratio variation in thrips with soldiers requires fine-scale genetic and demographic studies, as well as data from additional species (e. g., the K. waterhousei species complex).

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Scenario for the Origin and Evolution of Soldiers

Soldiers apparently originated soon after the host shift onto Acacia in the section Plurinerves from Acacia in the Juliflorae, after which two lineages, one with and one without soldiers, diversified onto the ancestors of Ac. harpophylla, Ac. cambagei, and the other microneurous Plurinerves species. In the lineage that developed soldiers, we have inferred that males commonly cofounded galls with females, relatedness and inbreeding levels were substantial within galls, and pressure from Koptothrips kleptoparasites was high. For unknown reasons, the galls induced by the thrips in this lineage were longer-lasting on the plants than those made by the lineages leading to K. ellobus, K. acaciae, K. maslini and K. rugosus. This increased gall persistence may have been related to a slower rate of nutrient input into the galls, leading to smaller galls, smaller broods, and an absence of physogastry. An extension of gall lifespan would have made galls vulnerable to invasion for a longer period, but it would also have made possible the evolution of two within-gall generations. At some point, the first-eclosing brood of the foundress would have had enough time to produce some offspring of their own within the gall. The origin of soldiers centers on an evolutionary trade-off between dispersal and staying, and for those who stay, options to reproduce, defend, or both. Staying within the natal gall would be favored by four main factors: (1) high costs to dispersal (see discussions in chapters on hover wasps, termites, and mole rats for further discussions on the costs of dispersal) and attempting to found one’s own gall, or (for males) mate with females after dispersal; (2) the ability of daughters of foundresses to increase fitness via personal reproduction or (for male protosoldiers) to mate with females in the gall; (3) the benefits of enhanced gall defense against Koptothrips; and (4) higher relatedness to disperser sibling gall mates saved via defense than to one’s own offspring that would be produced after dispersal. Along the lineage that evolved soldiers, these factors presumably tipped the balance towards adaptations of the first of the eclosing brood of a foundress to forego dispersal and specialize, behaviorally and morphologically, in within-gall reproduction and defense. Costs of dispersal and independent gall induction, which represent the ‘ecological constraints’ posited as central to the evolution of alloparental care (Brown 1987; Emlen 1992; Koenig et al. 1992), are expected to be high in such arid-zone inhabiting insects. However, we have no evidence as yet that such constraints were higher in the lineage leading to species with soldiers than in their sister-lineage that did not develop soldiers. Genetic and dissection data have shown that female soldiers reproduce, sometimes to a substantial degree (Chapman et al. 2002). From these findings we have inferred an ability of female proto-soldiers to reproduce, with especially high reproductive rates in lineages nearer to the inferred origin of soldiers (Chapman et al. 2002). Moreover, we have observed male soldiers mating with sisters on numerous occasions, and male proto-soldiers would have been the only mates available for proto-soldier females. These findings suggest that personal reproduction by females

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and males was an important component of the inclusive fitness equation mediating the evolution of soldiers, especially because staying within the gall to help defend it may often have led directly to death from Koptothrips. How much would colonies with proto-soldiers have gained in enhanced gall defense? In the evolution of soldiers, the first individuals to eclose in their natal gall would have been morphologically and behaviorally similar to foundresses, which observations and collections show are capable of defending against Koptothrips. After proto-soldiers became committed to remaining in the gall, there should have been strong selection for allocation of resources from dispersal adaptations to adaptations for reproduction, defense, or both. In other wing-polymorphic insects, wing reduction in females engenders higher reproduction, earlier reproduction, or both (Harrison 1980; Roff 1986; Roff and Fairbairn 1991; Roff and Bradford 1996); moreover, male wing reduction can involve earlier reproduction or higher allocation to weaponry (Crespi 1988). Each of these effects could have facilitated the rapid evolution of wing reduction in female and male proto-soldiers. Enlarged forelegs would have been favored by selection for more effective defense against Koptothrips, which would benefit one’s own offspring as well as offspring of the foundress and sisters. Behavioral experiments suggest that soldier propensity to defend is lower in more basal species, such that defensive motivation and ability may be inversely related to levels of soldier reproduction. Thus, relatedness among soldiers is not high enough to remove all between-soldier conflict over reproduction and defense, and given potentially high levels of personal reproduction, each soldier would prefer that a gall mate took on the dangerous task of gall defense. Moreover, there are higher numbers of soldiers in more basal species than in K. habrus and K. intermedius, so being less altruistic may incur lower costs in terms of successfully defending the gall. Microsatellite data provides evidence that relatedness was not higher to gallmates than to one’s own offspring, at least in part because high levels of inbreeding tend to reduce such relatedness asymmetries (Chapman 2003). However, relatedness was apparently high between gall mates at the origin of soldiers (Chapman et al. 2002), and inbreeding levels (FIS) of foundresses were also apparently substantial, on the order of 0.4–0.6. Such high inbreeding may also have made dispersing a more attractive option for incipient (still winged) protosoldiers, if it engendered higher relatedness to their own offspring than to those of the foundress. The diversification of species with soldiers involved two main trends: (1) the evolution of higher levels of reproductive division of labor in the lineage leading to the sister species K. habrus and K. intermedius, and (2) losses of the soldier caste in the lineages leading to K. rodwayi and K. xiphius. Stronger division of labor, involving higher skew and stronger defensive propensity, evolved in conjunction with relatively small gall size, low numbers of soldiers, and relatively low levels of the inbreeding coefficient FIS of dispersers. The evolution of fewer soldiers should be favored when it results in a higher number of dispersers (especially given the sharply limited brood capacity of the galls of K. habrus and K. intermedius). In turn, the presence of fewer soldiers may have selected for higher soldier motivation

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to defend, and higher soldier motivation should be favored when they reproduce less and specialize more strongly in altruistic defense. The lower FIS levels (on the order of 0.3) in K. habrus and K. intermedius may also have favored more highly developed altruism, since under lower inbreeding levels, soldiers may be less related to their own offspring, and so may be more inclined to alloparental focused behavior (Chapman 2003). The diversification of species with soldiers and their sister group is also intimately associated with patterns of host-plant use. Thus, the sister group to the lineage with soldiers, ((K. acaciae + K. ellobus) + (K. rugosus + K. maslini) ), exhibits the same pattern in host-plant relationships as the clade with soldiers: (1) a pair of sister species on Ac. cambagei (K. hamiltoni) and Ac. harpophylla (K. harpophyllae), and (2) use of a large number of closely related ‘microneurous’ Plurinerves Acacia species (by the K. rugosus and K. waterhousei sibling species or host races), and (3) additional species being found in Acacia species (e.g., Ac. orites, Ac. oswaldii, Ac. xiphophylla, Ac. melanoxylon, and Ac. calcicola) that are notably distant from these (Crespi et al. 2004). Moreover, both losses of soldiers apparently occurred in association with host-plant shifts to phylogenetically divergent Acacia hosts (Fig. 3.2). In K. rodwayi, this shift led to habitation of mesic areas, which may have reduced the strength of ecological constraint by making independent reproduction less costly (Kranz et al. 2002). In K. xiphius, the host-plant shift led to habitation of a highly arid region in the north of western Australia, which may have engendered life cycle changes, such as shorter-lived galls, favoring solitary life. All of the lineages that retained soldiers have remained on a suite of closely related Acacia except for K. intermedius, which appears to have undergone a major host-plant shift to Ac. oswaldii. Probably as a result of this shift, this species is highly unusual in several ways: (1) dispersers eclose within their natal gall rather than leaving as second instar larvae (as do all the other species with soldiers), (2) soldiers are partially winged rather than showing a near absence of wings, and wings are longer in soldiers that are smaller and have smaller forelegs (Crespi 1992a, 1992b), (3) galls without any soldiers are not uncommon, which is never the case in other species, and (4) it exhibits a unique pattern of sex ratios, with strong female biases in both soldiers and dispersers (Table 3.1). Eclosion in the gall, wingedness of foundress offspring, lack of soldiers, and a female bias in dispersers are also present in the solitary species K. rodwayi (which also exhibits a very similar gall to that of K. intermedius) and these traits have apparently evolved in parallel, since these two species are not sister taxa. These patterns suggest that K. intermedius and K. rodwayi have been subject to similar selective pressures, leading to lower soldier numbers in K. intermedius and, in K. rodwayi, their loss altogether. However, K. intermedius also exhibits especially high levels of reproductive skew between foundresses and soldiers, and a strong soldier defensive response. Might the benefits from producing increased numbers of dispersers sometimes outweigh benefits from defense by soldiers? In accordance with this hypothesis, K. intermedius exhibits the highest ratio of average soldier numbers (15) to average disperser numbers (60) of any species with soldiers.

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Conclusions

Our studies have several broad implications for the study of animal social evolution. First, gall-inducing thrips support the ‘factory-fortress’ model for the evolution of eusociality (Alexander et al. 1991; Crespi 1994; Queller and Strassmann 1998). Thus, they exhibit high relatedness due in part to their claustral habitat, strong pressure from natural enemies due to the extremely high value of their nest resource, and the ability to defend against these enemies, using weaponry that originated in a different selective context. These findings support the hypothesis that there are two more or less discrete ‘modes’ of eusociality: ‘factory fortress’ species that include gall thrips, gall aphids, some termites, snapping shrimp, some mole rats, and a species of ambrosia beetle; by contrast, ‘life-insurers’ or ‘forager-defenders’, include most eusocial Hymenoptera and some social birds and mammals (Choe and Crespi 1997). Alloparental care and eusociality have apparently been favored by considerably different selective pressures across these two modes of sociality, and broad-scale comparative studies on the causes of social evolution should consider them separately. Indeed, our findings suggest that the three main components of eusociality, behavioral, reproductive, and morphological divergence between morereproductive and more-helpful individuals, evolve in a different sequence for factory-fortress social forms than for eusocial taxa with foraging workers (Chapman et al. 2002; Thorne et al. 2003). Thus, in gall-inducing Acacia thrips, morphological and behavioral differences between soldiers and dispersers apparently evolved before strong reproductive skew; by contrast, the usual scenario for Hymenoptera is that behavioral divergence evolves in conjunction with high skew, and that morphological divergence can evolve only after these two conditions have been met (Wilson 1971; Bourke and Franks 1995). We have hypothesized that the factoryfortress route to sociality differs because defense trades off less strongly with reproduction than does energetically demanding foraging, and because defensive morphology makes reproductive domination by foundresses less likely (Chapman et al. 2002). Second, gall-inducing thrips with soldiers exhibit remarkable diversity in sex allocation ratio patterns, which are indicative of strong selection, and, we believe, parent-offspring conflict more or less resolved in different ways. We have suggested that foundresses use the timing and level of soldier and disperser sex ratio as a means to manipulate soldier alloparental and parental strategies towards their own interests. Coupled with our data on lack of relatedness asymmetry, these data suggest that one of the most important roles of haplodiploidy in social evolution is the ability to adaptively adjust sex ratios and produce males even when uninseminated. Finally, our findings show that the selective pressures responsible for the origin and diversification of soldiers in Australian gall thrips on Acacia involve complex evolutionary dynamics that reach across three levels: (1) relations to host plants, (2) intraspecific interactions between gall morphology, reproductive skew, brood size, sex allocation, defensive behavior, morphology, relatedness, and inbreeding, and (3) pressure from natural enemies. Elucidating the links between and within these

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levels benefits from a ‘model clades’ approach to making social-behavior studies multidisciplinary in a phylogenetic framework, and it should repay the perseverant student of social evolution with new insights into how cooperation and altruism evolve among all organisms.

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Queller DC, Strassmann JE (1998) Kin selection and social insects. Bioscience 48:165–175 Rhoden PK, Foster WA (2002) Soldier behavior and division of labor in the aphid genus Pemphigus (Hemiptera, Aphididae). Insectes Soc 49:257–263 Reeve HK, Westneat DF, Noon WA, Sherman PW, Aquadro CF (1990) DNA “fingerprinting” reveals high levels of inbreeding in colonies of the eusocial naked mole-rat. Proc Nat Acad Sci USA 87:2496–2500 Ross KG, Carpenter JM (1991) Phylogenetic analysis and the evolution of queen number in eusocial Hymenoptera. J Evol Biol 4:117–130 Roff DA (1986) The evolution of wing dimorphism in insects. Evolution 40:1009–1020 Roff DA, Fairbairn DJ (1991) Wing dimorphisms and the evolution of migratory polymorphisms among the insects. Am Zool 31:243–251 Roff DA, Bradford M (1996) The quantitative genetics of the trade-off between fecundity and wing dimorphism in the cricket Allonemobius socius. Heredity 76:178–185 Seger J (1983) Partial bivoltinism may cause alternating sex-ratio biases that favour eusociality. Nature 301:59–62 Shorthouse JD, Rohfritsch O (eds) (1992) Biology of insect-induced galls. Oxford University Press, Oxford Stannard LJ (1968) The thrips, or Thysanoptera, of Illinois. Bull Illinois Natl Hist Surv 29:215–552 Stern DL, Foster WA (1996) The evolution of soldiers in aphids. Biol Rev 71:27–79 Stern DL, Foster WA (1997) The evolution of sociality in aphids: a clone’s eye view. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 150–165 Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522 Thorne BL (1997) Evolution of eusociality in termites. Annu Rev Ecol Syst 28: 27–54 Thorne BL, Breisch NL, Muscedere ML (2003) Evolution of eusociality and the soldier caste in termites: influence of intraspecific competition and accelerated inheritance. Proc Natl Acad Sci USA 100:12808–12813 Trivers RL, Hare H (1976) Haplodiploidy and the evolution of the social insects. Science 191:249–263 Wade MJ, Breden FJ (1987) Kin selection in complex groups: mating structure, migration structure, and the evolution of social behaviors. In: Halperin Z, Chepko-Sade D (eds) Migration and social behavior. University of Chicago Press, Chicago, pp 273–283 Wcislo WT, Danforth BN (1997) Secondarily solitary: the evolutionary loss of social behavior. Trends Ecol Evol 12:468–474 Whitham TG (1979) Territorial behavior of Pemphigus gall aphids. Nature 279:324–325 Williams MAJ (ed) (1994) Plant galls: organisms, interactions, populations. Clarendon Press, Oxford Wills TE, Chapman TW, Kranz BD, Schwarz MP (2001) Reproductive division of labour coevolves with gall size in Australian thrips with soldiers. Naturwissenschaften 88:526–529 Wills TE, Chapman TW, Mound L, Kranz BD, Schwarz MP (2004) Description and natural history of Oncothrips kinchega, a new species of gall-inducing thrips with soldiers (Thysanoptera, Phlaeothripidae). Aust J Entomol 43:169–176 Wilson EO (1971) The insect societies. The Belknap Press of Harvard University Press, Cambridge Wilson EO (1975) Sociobiology. The Belknap Press of Harvard University Press, Cambridge

Chapter 4

The Ecology and Evolution of Helping in Hover Wasps (Hymenoptera: Stenogastrinae) Jeremy Field

Abstract In this chapter, I discuss the ecology and evolution of helping in hover wasps (Stenogastrinae), a tropical group that is uniquely suited for experimental studies in the field. I first outline the ecological benefits of helping that have been tested for in hover wasps, such as insurance advantages and direct fitness for helpers. I then discuss explanations for individual variation in helping decisions – why only some female offspring become helpers; and why some helpers work harder than others. Most of the chapter focuses on the hairy-faced hover wasp, whose behavioral ecology is best known, but I also discuss reproductive skew and task allocation in other species, and draw comparisons with other wasps where appropriate. The chapter ends with a comparison of the ecology of helping in hover wasps and that in cooperatively breeding vertebrates. The conclusion is that although helping can be understood using Hamilton’s inclusive fitness framework in both of these major taxa, the critical ecological factors differ fundamentally between them.

4.1

Introduction

It is now 40 years since Hamilton (1964) provided what is still a generally accepted framework for viewing the evolution of altruism. In that time, wasps, together with cooperatively breeding vertebrates, have been the most popular models for studying the evolution of the particularly extreme form of altruism known as eusociality, in which some individuals forfeit their own reproduction to rear the offspring of a queen or breeding pair. Although much of the emphasis since Hamilton’s paper has been on how variation in the coefficient of relatedness (r) could promote helping, the other two parameters in his famous inequality (rb>c), the costs (c) and benefits (b), are just as vital in determining whether helping is favored. It is therefore unsurprising that variation in relatedness alone has often proved to have limited power for explaining variation in critical features of social systems (e.g., Hughes et al. 1993; Jeremy Field Department of Biology and Environmental Science, University of Sussex, UK [email protected]

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Cant and Field 2001; Clutton-Brock 2002; Griffin and West 2003; Hammond and Keller 2004; but see Wenseleers and Ratnieks 2006). Measuring costs and benefits and determining the importance of specific ecological factors in the decision to help, is challenging. It usually requires experimental manipulation, ideally under natural conditions where results will be most meaningful. Stenogastrine wasps (Hymenoptera: Stenogastrinae), also known as hover wasps, are probably better suited than any other group of wasps and bees for experimental and observational studies of helping in the field. Yet because hover wasps are restricted to tropical areas, they were little studied until the early 1980s. At that time, research programs initiated by M.P. Hansell and S. Turillazzi began to reveal the full details of their biology, so that today at least a little is known about the natural history of six of the seven genera. In this chapter, I will examine the behavioral ecology and evolution of helping in hover wasps, thus illustrating their utility as research systems. I will focus primarily on the species best-studied in this respect, the Hairy-Faced Hover Wasp Liostenogaster flavolineata (Cameron), while drawing comparisons with other hover wasps and polistines where appropriate. I will then briefly summarize related material on hover wasps other than L. flavolineata, and finally consider general similarities and differences between the social systems of hover wasps and cooperatively breeding vertebrates.

4.2

Distinguishing Features of Hover Wasp Biology

Hover wasps comprise approximately 50 described species in seven genera (Carpenter and Starr 2000). They are medium-sized (1–2 cm long) black or brown and yellow wasps found in rainforest ranging from India to Papua New Guinea (Turillazzi 1991). Carpenter’s (1991) phylogeny, based on morphology and behavioral characters, placed them as the sister group of Polistinae+Vespinae, and subsequent molecular work casting doubt on that conclusion was controversial (Schmitz and Moritz 1998, 2000; Carpenter 2003). More recently, however, an independent molecular study based on four genes suggests that zethine potter wasps are the sister group of Polistinae+Vespinae, and that hover wasps are the sister group of all other vespids (Hines et al. 2007). This indicates that there have been two independent origins of eusociality among vespids, one in Polistinae+Vespinae and one in hover wasps. It also means that social traits shared between hover wasps and Polistinae+Vespinae represent convergence (Hines et al. 2007). Hover wasps have several features unique among wasps, which I summarize here based mostly on Turillazzi (1991) and references therein. Most noteworthy is the ‘abdominal substance’, a gelatinous white material synthesized in Dufour’s gland and produced from the tip of the adult female’s abdomen. This substance, originally assumed to provide larval nutrition, is now thought to function as an oviposition tool and substrate on which small larvae rest, as well as a depository for food provisions. Instead of ovipositing directly into a cell, a female first produces a ball of abdominal substance. She then holds the ball in her mouth while she bends her abdomen under her thorax and lays an egg on it. The egg plus abdominal substance is then placed in the cell (see photographs in Turillazzi 1991). The abdominal

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substance is also used to construct the ant guards that protect the nests of some hover wasps. Hover wasp larvae lie curled around the long axes of their cells, unlike the larvae of polistines and vespines, which lie longitudinally with their heads towards the cell entrances. Larvae are provisioned progressively like those of polistines and vespines, but instead of placing food directly onto the larval mouthparts, adults place it onto the abdominal substance in cells containing small larvae, or onto the middle of the bodies of larger larvae as they lie coiled in their cells. Hover wasps nest typically in dark, hidden places near water: under overhanging earth banks, rocky overhangs, caves, etc. Nests lack the petiole of polistines and vespines, and are often highly camouflaged. Nest structure is incredibly diverse compared to most other groups of wasps, even within a single genus such as Liostenogaster, such that species are often easier to identify from their nests than from characteristics of the adults (see Turillazzi 1991 for examples). Hover wasps appear to have few specialized natural enemies, with major predators being generalists, notably ants and hornets. At least one specialized parasitic wasp is known, however (Coster-Longman et al. 2002; pers. observ.). Adult hover wasps are aggressive only towards conspecifics and enemies smaller than themselves: when confronted with a larger threat such as a hornet or human, they immediately flee. Hover wasp social groups are small; mean group sizes range between 1 and 4 females, with individual groups almost never exceeding ten females (Turillazzi 1996). Initially thought to vary in their level of sociality, all species are now thought to be eusocial in the sense that there is a clear reproductive and usually behavioral division of labor whenever group size is greater than one. No obligate socially parasitic species have been found. Further details of hover wasp biology, including what is known of male behavior, can be found in Turillazzi (1991).

4.3

The Hairy-Faced Hover Wasp Liostenogaster flavolineata as a Model System

Research on L. flavolineata began with the monumental PhD thesis of Charlotte Samuel (1987). Her work included long-term monitoring of nests with individually marked wasps, and the first detailed description of the L. flavolineata social system, establishing a baseline on which later work has been built. L. flavolineata has primarily been studied near Gombak (bridge site and gazebo sites approximately 10 km apart) and near Fraser’s Hill, a higher altitude area approximately 60 km from Gombak (1,000 m a.s.l.). All of these sites are in peninsular Malaysia.

4.3.1

Summary of Nesting Biology

L. flavolineata builds mud nests consisting of a single open comb of cells (Fig. 4.1), similar in basic form to the paper nest of Polistes. Nests are usually initiated by a single foundress, but a second female occasionally joins her before any offspring

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Fig. 4.1 Mud nest of L. flavolineata with individually marked adults. Developing offspring are just visible in some of the inner cells. Photo: A Cronin

Fig. 4.2 Part of a cluster of L. flavolineata nests under a bridge. Each of the pale, roughly circular structures is a separate nest. Photo: J. Field

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reach adulthood (Samuel 1987). Females are thought to be unusually specialized predators, feeding their larvae exclusively on winged ants and termites (Samuel 1987). Offspring development lasts approximately 100 days (Samuel 1987; J. Field unpubl. data), considerably longer than the 40–50 days typical of polistines and hover wasps of other genera (Hansell 1982, 1987b; Turillazzi 1985; Reeve 1991). Brood-rearing occurs throughout the year at the sites where L. flavolineata has been studied, but there still appears to be seasonal variation in parameters such as the frequency of nest-founding, mean group size, and the mean number of immature offspring being reared (Samuel 1987; Shreeves and Field 2002; J. Field and G. Shreeves, unpubl. data). Many female offspring remain on their natal nests as helpers, which forage to feed the immature offspring. Females may, however, leave at any time. Many such females initially become nest-less floaters, but subsequently pursue alternative strategies (Samuel 1987; Field et al. 1999). These strategies include nest-founding, usurping a lone female or adopting a nest that has fallen vacant after its previous residents have disappeared, or occasionally joining a pre-existing group (Samuel 1987; Field et al. 1998a). Male offspring usually leave their natal nests soon after reaching adulthood, although some become nest-residents (J. Field, unpubl. data). There can be up to 90 cells and ten females resident on a nest, close to the maxima recorded for hover wasps (Turillazzi 1996). Brood-rearing cells are repeatedly re-used and nests are perennial, sometimes persisting for 10 years or more (J. Field, unpubl. data). The number of cells therefore reflects the largest number of offspring reared simultaneously during the history of the nest rather than the current number being reared, and more than 50% of cells are typically empty at any one time (Field et al. 1998a). This suggests that the mechanism stimulating oviposition may not be the presence of empty cells as has been suggested for Polistes (Karsai et al. 1996).

4.3.2

Gerontocracy and Colony Genetic Structure

Observation of an L. flavolineata nest usually reveals a behaviorally dominant female that rarely leaves the nest, never forages for larval provisions and is more aggressive than other group-members (Samuel 1987; Field and Foster 1999). Sumner et al. (2002) used microsatellite markers to show that the dominant lays all or almost all of the eggs at any one time. Subordinates lay a small proportion (∼10%) of the male eggs, perhaps because they tend to be more closely related to the dominant’s daughters than to her sons. Genetic data suggest that females mate only once and that there is no inbreeding, consistent with mating not being observed on the nest (Sumner 1999; Sumner et al. 2002; Bridge 2005). Samuel’s (1987) long-term monitoring of a single nest suggested that the dominant tended to be the oldest female in the group, replaced on her death by the next-oldest female, a system termed ‘gerontocracy’ by Strassmann and Meyer (1983). Bridge and Field (2007) have recently confirmed the generality of this pattern in L. flavolineata by experimentally removing successive dominants from nests with

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residents of known age. After 87% of 69 removals, the next-oldest female indeed inherited the dominant position. The gerontocracy in L. flavolineata appears to contradict a recent model which predicts that in tropical taxa, where colonies outlive individuals, replacement dominants should be younger rather than older individuals (Tsuji and Tsuji 2005). It is possible that age represents an arbitrary convention for deciding dominance, although this begs the question of why the same convention is used in multiple taxa (Tsuji and Tsuji 2005). The immatures from eight out of the 13 nests genotyped in detail by Sumner et al. (2002) comprised two different sibships, indicating that at least some of a previous dominant’s offspring are reared through after she dies. The remaining five nests contained only a single sibship. The first genetic study of L. flavolineata was allozyme-based and estimated mean within-nest adult female relatedness as 0.22 ± 0.10, the lowest then known for a primitively eusocial insect (Strassmann et al. 1994). Sumner et al. (2002) took wasps from under the same bridge sampled by Strassmann et al. 5 years earlier, and obtained a considerably higher estimate of 0.52 ± 0.05 using hypervariable microsatellite loci. Sumner (1999) obtained a similar estimate of 0.45 ± 0.1 using a smaller sample from the nearby Gazebo site, and Bridge (2005; Field et al. 2006) obtained an estimate of 0.46 ± 0.08 from Fraser’s Hill. Overall, these data suggest that mean relatedness is normally 0.4–0.5, within the range typical for other primitively eusocial wasps (Ross and Carpenter 1991). Female nest-mates are probably a mixture of mainly sisters, auntniece, mother-daughter or cousins, primarily reflecting the gerontocratic inheritance system (Field et al. 2006). The relatedness estimates that have been obtained for three other hover wasps are also fairly high: 0.46 ± 0.054 and 0.56 ± 0.19 in Parischnogaster alternata; 0.33 ± 0.05 in P. mellyi; and 0.43 ± 0.13 in Eustenogaster fraterna (Strassmann et al. 1994; Landi et al. 2003; Fanelli et al. 2005; Bolton et al. 2006).

4.3.3

Advantages of L. flavolineata for Experimental Work

L. flavolineata has most of the same advantages as Polistes as a model system, including behavioral flexibility and an open comb of cells upon which all adult behavior can be observed (Fig. 4.1). In addition, however, L. flavolineata has three advantages not typical of Polistes, whose practical value cannot be over-emphasized. It is one of three hover wasp species in which nests are often clustered together in groups of sometimes 100 or more (Fig. 4.2). Large clusters occur naturally under rocky overhangs but are also found on man-made structures such as under bridges and on the ceilings of culverts that carry streams under roads (Samuel 1987; CosterLongman et al. 2002; J. Field, pers. obs.). Much smaller clusters and isolated nests are also common, and nests additionally occur attached to plant roots that hang exposed beneath overhanging soil banks. Large clusters of nests associated with accessible man-made structures are ideal for research purposes. They allow many social groups to be studied under the same environmental conditions, and this is facilitated by the lack of aggression towards humans. The individually marked wasps on a group of 100 nests can be censused in less than an hour, a considerable

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advantage compared to the more spatially separate nests typical of polistines. A second major practical advantage provided by hover wasps is the low rate of nest predation. This is especially true of L. flavolineata, whose robust mud nests are rarely damaged by hornets (Samuel 1987; Coster-Longman et al. 2002). If a group of 100 L. flavolineata nests is experimentally manipulated then monitored for 3 months, more than 95 will typically still be present at the end of the experiment. A third advantage is that hover wasp groups remain continuously small, allowing all group members to be kept individually marked over long periods of time: there is not the sudden increase in group size that occurs after worker emergence in temperate wasps such as Polistes. One disadvantage for some purposes is that offspring development lasts approximately twice as long as Polistes.

4.4

Ecological Benefits of Helping

A fundamental question in L. flavolineata, as in other primitively eusocial animals, is why some individuals choose to become helpers on their natal nests instead of leaving to reproduce independently. L. flavolineata helpers are less closely related to both female and male brood than they would be to their own offspring (Sumner et al. 2002). This suggests that there must be ecological advantages to becoming a helper. In the following three sections, I will review studies that have tested for such advantages in L. flavolineata.

4.4.1

Costs of Nest Initiation

Independent nesting involves paying two costs associated with nest initiation: the cost of finding a suitable nest site and the cost of building a new nest. Potentially, this could explain why females opt to become helpers. In many wasps and bees, a helper avoids only some of the nest-building costs, such as those involved in producing a nest petiole or a protective nest envelope. If her decision to help leads to the group rearing more offspring, then new cells may have to be built to house those offspring, just as an independent nester will have to build new cells. In L. flavolineata, however, a female that chooses to help may avoid more of the costs of nest initiation than in most wasps and bees. Because more than half of the cells in a typical nest are empty at any given time, any extra offspring that a helper rears may be placed in these pre-existing cells (Field et al. 1998a). Furthermore, the mud nest of L. flavolineata may be unusually costly to build: nest weight per cell is roughly 50 times that of a Polistes nest, although costs of processing mud versus wood pulp are unknown (Field et al. 1998a). L. flavolineata nests occasionally fall vacant when their owners disappear (Samuel 1987; pers. obs.). If independent nesting is constrained primarily by the costs of nest initiation, helpers should adopt vacant nests, as has sometimes been

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observed (Samuel 1987; Field et al. 1999). Aggregated clusters of L. flavolineata nests provide an ideal opportunity to test this hypothesis (Fig. 4.2). In two experiments, helpers were provided with easily accessible vacant nests, either by removing the residents from one-third of the nests in the cluster, or by adding nests taken from a different site. In each experiment, less than 5% of the vacancies were filled by helpers from unmanipulated nests, even though the ratio of helpers:vacant nests was > 8:1 (Field et al. 1998a). Helpers did visit vacant nests, but chose not to adopt them. Thus, although the costs of nest initiation may contribute towards the decision to become a helper, they do not seem to provide a complete explanation (see also Bull and Schwarz 1996 in an allodapine bee). These results are opposite to those of analogous experiments on cooperatively breeding birds, in which helpers immediately left their groups to adopt experimentally provided territorial vacancies (Komdeur 1992; Pruett-Jones and Lewis 1990; Walters et al. 1992). Together, these findings suggest that a territory is a more valuable resource for a vertebrate than is a nest for a wasp (Field et al. 1998a).

4.4.2

Insurance-Based Advantages of Helping

Insurance-based advantages depend on what happens to a female’s investment after she dies. In hover wasps and other eusocial vespids, offspring require continuous adult care during their development. This is partly because larvae are fed gradually as they grow: the death of its carers will mean starvation for a partially fed larva. Even fully grown larvae and pupae remain vulnerable, however. Without the second component of adult care, protection, they often fall prey to generalist predators such as ants. It is therefore a paradoxical feature of social wasp life-histories that adult carers are short-lived compared to the development period of their dependent offspring. Lifespans may be short because foraging is a risky activity. As in polistines, fewer than 50% of independent-nesting L. flavolineata females can expect to survive long enough to bring any offspring through to adulthood: the remainder will have zero reproductive success (Samuel 1987; Queller 1996; Field et al. 1998a, 2000). This may explain why so few of the vacant nests were adopted in the experiment of Field et al. (1998a): a vacant nest is of little value if there is only a small chance or rearing independent offspring in it. Nesting independently is clearly a risky option for a female wasp, but will a helper fare any better? A helper also has to forage, and in L. flavolineata has the same life expectancy as an independent nester (Field et al. 2000). The critical difference is that even if a helper dies young, her investment may be preserved through various forms of insurance that are unavailable to independent nesters. The first form occurs because when she reaches adulthood, a helper is usually on a nest that already contains partially reared offspring. Unlike an independent nester, she does not have to start rearing offspring from the egg stage (Queller 1989). It is therefore more likely that some of the offspring she helps to rear will have reached adulthood before the group fails. The second reason that an early death need not mean total

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failure for a helper is that while she was present as a forager, her dominant relative did not have to carry out risky foraging herself, and other high-ranking helpers were able to decrease their foraging effort partially (Cant and Field 2001; Field et al. 2006). Through prolonging her relatives’ lifespans, the helper also reduces the risk that the whole group will fail (see Reeve 1991; Queller 1996). This advantage, known as ‘survivorship insurance’, will be largest for the first helper (Nonacs 1991). Consistent with survivorship insurance, groups that are made smaller experimentally do take longer to fail in L. flavolineata (Shreeves and Field 2002). The third potential insurance advantage for helpers, and the one best investigated in L. flavolineata, is known as ‘Assured Fitness Returns’ (Gadagkar 1990). The idea is straightforward: after an independent nester dies, her part-reared offspring are doomed. In contrast, after a helper dies, the offspring she contributed to may be brought to maturity by surviving nest-mates (Strassmann and Queller 1989; Gadagkar 1990). As in most primitively eusocial insects, each additional L. flavolineata helper allows the group to rear a few more offspring (Field et al. 2000; Shreeves and Field 2002). When a helper dies, therefore, the reduced group is left with extra offspring compared to the number that such a group would normally rear (Fig. 4.3). Experimental removal of helpers to mimic natural deaths showed that these extra offspring are indeed almost entirely reared through to maturity, effectively preserving the dead helper’s investment (Field et al. 2000). In contrast, experimental removal of independent nesters not surprisingly led to the almost complete failure of their part-reared offspring. Even allowing for the fact that independent nesters are more

Fig. 4.3 Illustration of assured fitness returns. The solid line shows the observed positive relationship between group size and the total number of offspring being reared in L. flavolineata. Dashed lines show numbers of offspring reared by groups of 4 and 5 females, the difference on the y-axis representing the investment of the fifth individual. If that individual dies, the reduced group of four will be left with extra offspring on top of the number that a group of four would normally rear. In L. flavolineata, the extra offspring are almost all reared through, so that helpers do indeed have assured fitness returns (Field et al. 2000)

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closely related than helpers to the offspring being reared, they would have to be approximately 1.7 times as productive as helpers to compensate for failure of their offspring when they die (Field et al. 2000). To put this in context, Hamilton’s (1964) famous ‘haplodiploidy’ hypothesis gave helpers a 1.5 times productivity advantage. How a reduced group manages to rear the extra offspring left after a helper dies is uncertain: remaining adults do not seem to increase their foraging rates, and offspring development time is the same as on control nests (Field et al. 2000). Some of the extra offspring will be fully fed larvae or pupae that require only protection to complete their development: remaining adults can provide this through their presence alone. The extra pupae should themselves increase the shortterm rate of helper recruitment to a reduced group, making it easier to rear extra smaller offspring through to adulthood. A third mechanism is suggested by finding that the very smallest extra offspring (eggs and tiny larvae) are not reared through after a helper’s death. These may be sacrificed to feed the larger offspring. Effectively, when left with a package of extra offspring that it cannot afford to rear, a reduced group may rear the larger, more valuable offspring by feeding them with the smaller, less valuable offspring (Field et al. 2000). Even if some larvae receive less than the normal amount of food, investment is preserved so long as resulting adults suffer a decrease in fitness that is no more than proportionate with the reduction in food.

4.4.3

Direct Fitness for Helpers Through Inheritance

Although the dominant lays almost all of the eggs on an L. flavolineata nest, helpers have a chance of eventually inheriting the dominant position themselves. Helpers are in an age-based queue, each waiting until she is the oldest living female and becomes the dominant (Samuel 1987; Bridge and Field 2007). Age-based queuing is common in primitively eusocial animals, and queue dynamics are predictable (Fig. 4.4): Kokko and Sutherland 1998; Field et al. 1999; Shreeves and Field 2002). In particular, the further a female is from the front of the queue, the smaller her chance of surviving to inherit. The obvious alternative to remaining in the queue is for a female to leave her natal nest and nest independently. She can then immediately become an egg-layer, but will have no helpers herself unless she is joined by other females or survives to produce adult offspring. In contrast, a queuing female stands to inherit not just the egg-laying position but also a group of younger females that will rear her offspring and provide insurance if she dies (Shreeves and Field 2002). Since offspring production increases linearly with group size in L. flavolineata, this is a significant advantage. The relatively small group sizes found in hover wasps mean that the chance of inheritance may be unusually high (Fig. 4.4). Furthermore, unlike temperate wasps, waiting times for hover wasp helpers are not constrained by the arrival of winter. Overall, direct fitness may be a relatively large component of total fitness for hover wasp helpers, although this has yet to be quantified. One question this

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Fig. 4.4 Estimated relationship between position in the queue and chance of surviving to inherit the dominant (rank 1) position. The filled circles assume that all individuals have equal expected lifespans and constant mortality rates, so that the probability of inheritance is simply 1/n, where n = group size. The open circles are based on the observed relationship between mortality rate and queue position in L. flavolineata, in which higher-ranked individuals live longer than lower-ranked individuals (re-drawn from Field et al. 1999)

raises is whether a female would do best to remain in the group but not forage, thus minimizing her mortality risk while maximizing her chance of surviving to inherit. It is possible that other group members would punish such cheats or expel them from the group (see Mulder and Langmore 1993; Balshine-Earn et al. 1998). In addition, although foraging probably has significant personal costs, it has indirect fitness benefits through increased production of related offspring, and perhaps also direct benefits (Kokko et al. 2001). The interplay between the various costs and benefits of actively helping is an interesting area for future research that will be discussed further below, when considering individual variation in helping effort (Sect. 4.5.3).

4.5 Individual Variation in Helping Decisions Insurance advantages, indirect benefits through rearing relatives, and resource inheritance through queuing are factors that could help to explain why females choose to become helpers. A further question, however, is why there is variation. First, why do some females choose to help while others leave their natal nests and

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pursue other strategies? One possibility is that this represents a parental bet-hedging strategy. Another, not mutually exclusive explanation is that different decisions are adaptive for the individual offspring concerned. A second, related question is why do some helpers appear to work harder than others? Before discussing whether decision-making is adaptive, I will briefly outline the evidence that some female offspring do indeed leave. The proportion of female offspring that choose to leave their natal nests is hard to quantify in L. flavolineata because of the difficulty of distinguishing between leaving and death. Samuel (1987) implies that around 70% of 230 newly emerged females disappeared from their natal nests, the other 30% becoming helpers. Of those that disappeared, 22% were seen subsequently, so that 15% is a minimum estimate of the true proportion leaving. Two-thirds of the definite ‘leavers’ initially became nest-less floaters, while others immediately built new nests, adopted vacant nests, or joined lone foundresses. Samuel (1987) does not give the timescale over which females disappeared, and it is not clear whether she took possible effects of marking into account. Field et al. (1999) examined the fates of 126 newly emerged females whose decisions were unlikely to have been affected by marking. They found that on average, 2.5% of females disappeared per day. There was no indication that this rate changed during the first month of life, but older females disappeared at the significantly lower rate of 1.2% per day. One explanation for this difference is that there is a ‘leaving window’ early in life, while another is simply that younger females have higher mortality rates, although this did not agree with the fact that they spent more time on the nest than older subordinates (Field et al. 1999). Only 13% of females that disappeared were seen again. Coster-Longman and Turillazzi (1998) could distinguish between leaving and death in their captive population of another hover wasp, Parischnogaster mellyi. They found that 75% of newly emerged females left their natal nests, supporting the idea that many of the disappearances seen in the wild truly represent leaving.

4.5.1

Queue Length and Leaving Decisions

A female’s decision to stay or leave might depend on her phenotype or genotype as well as environmental conditions including the social environment on her natal nest. One key variable could be queue length, the number of older females already on the nest. A newly emerged female will start at the end of the queue, and her chance of inheriting the dominant position will decline exponentially with decreasing rank (Fig. 4.4). The positive relationship between group size and both productivity and insurance benefits in L. flavolineata will tend to counteract this effect: females that do inherit will enjoy greater reproductive success in larger groups (Field et al. 1999; Cant and Field 2001; Shreeves and Field 2002). Nevertheless, the net effect might be a threshold queue length above which females would do better to leave (Shreeves and Field 2002). To test this idea, Field et al. (1999) experimentally reduced the queue lengths on half of the nests

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in two clusters, but found that newly emerged females were no less likely to disappear from manipulated nests than controls. This suggests that the disadvantage of starting from the end of a longer queue may be approximately balanced by advantages that are positively correlated with group size (Shreeves and Field 2002). However, a threshold queue length above which newly emerged females leave their natal nests might be revealed by experimentally lengthening (rather than shortening) natural queues.

4.5.2

The Subfertility Hypothesis

The subfertility hypothesis is another potential explanation for variation in leaving decisions. It suggests that females of relatively low quality choose to become helpers because they would achieve little reproductive success if they attempted independent reproduction (West-Eberhard 1975; Craig 1983). Effectively, the cost of helping, in terms of own reproduction lost, is low for such females. A general problem for the subfertility hypothesis is that low-quality females may also make poor helpers (Craig 1983; Queller 1996): helpers must carry out the same tasks as independentnesting females, including nest-building and foraging. An exception, however, is egg-laying. Females with a reduced ability to lay eggs but with normal capabilities otherwise, might choose to become helpers. Field and Foster (1999) tested the ability of L. flavolineata helpers to lay eggs by removing the dominant and all but one focal helper from 22 nests. The focal helpers thus forced to nest alone soon mated and developed ovaries characteristic of dominants. While far from a quantitative comparison of helpers and independent nesters, this experiment shows that helpers are generally not unconditionally physiologically constrained. Also arguing against subfertility as an explanation for helping in L. flavolineata and many other primitively eusocial insects is the gerontocratic system of inheritance: today’s ‘subfertile’ helpers are tomorrow’s dominant egg-layers. One way around this might be if low-quality helpers have higher mortality rates, and are therefore less likely to ever become dominants. To the extent that size reflects quality, there is no evidence for this in L. flavolineata: rates of disappearance are independent of size, and dominants are not systematically larger than subordinates (Field et al. 1999; Sumner et al. 2002). In a study of Polistes fuscatus, smaller females were actually more likely than larger females to disappear from their natal nests (Reeve et al. 1998b). This is opposite to the predictions of the subfertility hypothesis because disappearing females are thought to be those that overwinter and found new nests in spring. In contrast, Yanega (1989) found that larger female offspring were more likely to leave and overwinter in the sweat bee Halictus rubicundus, but he suggested that the underlying cause could be a seasonal increase in offspring size rather than size-based decision-making. Whereas Yanega re-sighted a large proportion of leavers the following spring, interpreting the data for Polistes and Liostenogaster is complicated by the problem of not being able to distinguish whether most disappearing females had truly left or had simply died. This could

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make it harder to detect adaptive patterns, and observed patterns could even reflect size-related mortality rather than individual decision-making. Further progress in this area awaits the development of tracking devices suitable for individual wasps, or might involve captive populations such as those studied by Coster-Longman and Turillazzi (1998). The subfertility hypothesis seems worthy of further investigation in primitively eusocial insects. There is a dearth of experimental tests to date, perhaps because of the difficulty of measuring quality or fertility.

4.5.3

Individual Variation in Helping Effort

Helping is not an all-or-nothing decision. In eusocial and cooperatively breeding societies there is substantial variation in how hard individual helpers work (CluttonBrock et al. 2000; Cant and Field 2001). Initial attempts to understand this variation focused on the prediction that more help should be given to closer relatives, but with mixed results (e.g., Clutton-Brock et al. 2000; Queller et al. 2000; Griffin and West 2003). In L. flavolineata, for example, helping effort is not correlated with relatedness, even after controlling for other variables (Field et al. 2006). In insects, the lack of support for kinship-based nepotism in general may reflect informational constraints, or prohibitive costs to the group (Keller 1997; Hannonen and Sundström 2003). The failure to explain much of the variation in helping effort using relatedness has led some to question whether kin selection truly provides a general explanation for helping (Clutton-Brock 2002; Griffin and West 2002). Cant and Field (2001, 2005) developed models in which variation in helping effort primarily reflects variation in the costs of helping. Helpers face a fundamental trade-off: by working harder to rear the offspring of a relative, they simultaneously decrease their own future survival and reproductive success through inheriting breeding positions. Because individuals with greater expected future fitness have more to lose, they should work less hard (Cant and Field 2001). Social queues, where individuals inherit breeding positions in a predictable order, are ideal for testing this hypothesis because they lead to systematic differences in expected future fitness. In particular: (1) individuals nearer the front of the queue are more likely to inherit (Fig. 4.4), and (2) if larger groups are more productive, an individual waiting in a longer queue can expect greater reproductive success should she succeed in inheriting. Consistent with these differences, Cant and Field (2001) found that subordinate co-foundresses in Polistes dominulus allocated a smaller proportion of their time to risky foraging if they were nearer to the front of the queue, or if they were in a larger group. In both cases, individuals with more to lose were prepared to work less hard. These effects were only correlative, however. Position in the queue cannot be deduced a priori in P. dominulus, so that it cannot easily be manipulated. The strict age-based queue in L. flavolineata allows a more convincing test: by knowing their relative ages, it is possible to order females precisely in the queue. Recent experiments in which queue position and group size were experimentally manipulated show that L. flavolineata helpers adjust their foraging

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effort just as predicted from the life-history perspective of Cant and Field. Helpers worked less hard after being promoted in the queue, but worked harder if their groups were made smaller (Field et al. 2006). The absence of any correlation between helping effort and relatedness might primarily reflect the inability of helpers to distinguish variation in relatedness at the individual level (Keller 1997). In contrast, group size and position in the queue may provide easily discernible indications of the future fitness that a helper stands to lose. Helpers may thus respond to variation in individual future fitness, while being forced to respond only to the average relatedness. How females determine their position in the queue is unknown. In small groups, one possible mechanism might be for a female to learn the identities of the other females that were already present when she first reached adulthood (see Tibbetts 2002). The fewer of these that remain alive, the nearer to the front of the queue she must be if queuing is age-based. A second possibility is that cues such as cuticular hydrocarbon composition are correlated with age, and therefore with queue position (see Sledge et al. 2001; Cuvillier-Hot et al. 2004; Turillazzi et al. 2004). Females might compare their own cues with those of nest-mates.

4.5.4

Individual Variation in Aggression

Position in the queue should affect a female’s willingness to perform any act that might jeopardize her future fitness, not just foraging. A possible example is aggression towards nest-mates. Like foraging, aggression may be risky, if it can lead to the aggressor’s death or injury, but unlike foraging, aggression could also increase the actor’s future direct fitness through queue-jumping. Cant et al. (2006) showed theoretically that if aggression functions to test or challenge individuals ahead in the queue, or to deter challenges from individuals further back, high-ranking subordinates should be more aggressive. Most interactions on unmanipulated L. flavolineata nests are apparently mild antennations of one female by another, but this can escalate into chasing and biting (Cronin and Field 2007b). Cronin and Field (2007b) obtained results consistent with Cant et al.’s model in that high-ranking subordinates tended to both initiate and receive more interactions, although this was partly because high rankers spent more time on the nest. Cronin and Field (2007a) found a similar pattern in defensive behavior: higher-ranked individuals were the most likely to defend the nest against foreign conspecifics.

4.6

Helping in Hover Wasps Other than L. flavolineata

Although L. flavolineata is the only hover wasp in which experimental manipulations have been used to study costs and benefits of helping, the social biology of other species has been examined in more or less detail (see summary and references in Turillazzi 1991). Here, I will briefly summarize just two aspects of these studies:

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first, reproductive skew; and second, the reduced behavioral division of labor that seems to occur in Eustenogaster fraterna.

4.6.1

Reproductive Skew in Hover Wasps

Whenever there is genetic heterogeneity among the individuals in an animal society, relatedness asymmetries between group members and potential offspring may lead to conflicts of interest as different individuals simultaneously attempt to maximize their genetic profit (Ratnieks and Reeve 1992). Reproductive skew, the degree to which reproduction is shared among the members of a society, is one such conflict that has recently attracted particular attention. The distribution of reproduction among group members may range from complete equality (low skew) to monopolization by a single breeder or dominant (high skew). Over the past decade, several models have been formulated to examine how skew may be affected by genetic, ecological, and behavioral factors: for reviews, see Johnstone (2000), Magrath and Heinsohn (2000), Reeve and Keller (2001). Concessions models are built on the assumption that groups contain a single dominant breeder that has complete control over subordinate reproduction (Vehrencamp 1983; Reeve and Ratnieks 1993; Kokko and Johnstone 1999; Ragsdale 1999). This dominant individual has the option of yielding a reproductive concession to a subordinate in exchange for its cooperation. In contrast, tug-of-war models assume that dominants have incomplete control of subordinates, and groupmembers channel resources into intra-group competition over reproduction (Reeve et al. 1998a). All female hover wasps are potential reproductives, but the small groups and small physical nest structures suggest that dominants could have complete control over reproduction, as in the ‘concessions’ framework. Hover wasps therefore represent potentially useful model systems, and genetic markers have been used to estimate skew in L. flavolineata, Parischnogaster mellyi and P. alternata (Sumner et al. 2002; Fanelli et al. 2005; Bolton et al. 2006). Despite intraspecific variation in some of the parameters predicted theoretically to influence skew, however, and despite the somewhat lower average relatedness in P. mellyi, skew in all three species is consistently extremely high, close to complete monopolization of reproduction by the dominant. Individual groups with lower relatedness do occur, but generally still maintain high skew. These results are contrary to initial speculation that hover wasps might have relatively low skew (Sherman et al. 1995). Within the framework of the concessions models, at least two factors could account for consistently high skew. The first is strong ecological constraints on independent nesting: a lone L. flavolineata female has at most a 50% chance of surviving to produce adult offspring (Samuel 1987; Field et al. 2000). The concessions models predict that strong constraints will induce helpers to accept a high skew (Reeve and Ratnieks 1993). The second factor is the relatively good chance that helpers have of eventually inheriting dominance

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themselves: effectively, skew is lower when considered over a helper’s entire lifespan (Fig. 4.4; Sumner et al. 2002). Life-history-based models of skew predict that such delayed benefits can stabilize a high skew (Kokko and Johnstone 1999; Ragsdale 1999). Although somewhat unsatisfying because of their qualitative nature, these conclusions are mirrored by studies of reproductive skew in Polistes (Field et al. 1998b; Queller et al. 2000; Seppa et al. 2002; but see Reeve et al. 2000; reviewed by Field and Cant, in press). Further progress in this area will require experimental manipulation of key parameters such as ecological constraints and relatedness (e.g., Langer et al. 2004), together with interspecific comparative analyses.

4.6.2

Task Allocation in Eustenogaster fraterna

Some hover wasps, such as species of Stenogaster and Anischnogaster, have considerably smaller average group sizes than L. flavolineata, with most nests having just a single female resident at any one time (e.g., Spradbery 1975; Turillazzi and Hansell 1991). This might reflect weak constraints on independent nesting so that most offspring leave their natal nests, or environmental conditions that lead to high adult mortality rates relative to the birth rate. Peculiarities of nest structure that limit maximum nest size might also contribute (Hansell 1987a; Turillazzi 1990). Nevertheless, in the minority of groups that have multiple female residents, there is still a clear behavioral division of labor in these species, comprising one or more foragers and a dominant female that rarely leaves the nest (Turillazzi and Hansell 1991). Recently, however, an apparent exception to this pattern has been described in E. fraterna (Francescato et al. 2002). In E. fraterna, relatedness is fairly high and group size not as small as in Stenogaster and Anischnogaster (Landi et al. 2003). There seems to be only a single egg-layer as in other hover wasps, but unusually, the egg-layer carries out much of the risky foraging. This contrasts with most other primitively eusocial wasps, including other hover wasps such as the congeneric E. calyptodoma, in which the egg-layer rarely leaves the nest and never forages for larval provisions (Hansell 1987b). Other exceptions to this rule appear to be very small groups of some Polistes, where dominants carry out some of the foraging, and xylocopine bees in which an older egg-layer does most or all of the foraging while a non-egg-layer guards the nest entrance (e.g., Lorenzi and Turillazzi 1986; Field et al. 1998b; Hogendoorn and Velthuis 1999). The situation in E. fraterna superficially resembles that in some co-operatively breeding vertebrates, in which breeders continue to forage in the presence of helpers. By working less hard and thereby forcing the dominant to work harder, helpers may increase their chance of inheriting the dominant position (Francescato et al. 2002). Francescato et al.’s data suggest that the behavioral division of labor may even vary between nests of E. fraterna, and more work on this system could be of great interest.

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Conclusions: Helping in Stenogastrine and Vertebrate Social Systems—Similarities and Differences

In eusocial wasps and bees, helping takes a form similar to that in many cooperatively breeding vertebrates, particularly birds: by foraging to feed the breeder’s offspring, helpers increase the number of offspring successfully reared. In most wasps, such as L. flavolineata, however, the increase results partly from increased clutch size, whereas in vertebrates it typically results from a larger proportion of offspring reaching maturity from a fixed initial clutch (e.g., Field et al. 2000 and Shreeves et al. 2003 in wasps; Heinsohn and Cockburn 1994 and Wright 1997 in vertebrates). In part, this may reflect a limitation on clutch size in vertebrates that produce relatively large offspring, compared to the smaller, less costly offspring of insects. In wasps, breeders completely cease foraging in the presence of helpers, almost certainly increasing their own and often the group’s survivorship, paralleling the ‘load-lightening’ that occurs in many cooperatively breeding birds (e.g., Reeve and Nonacs 1997; Shreeves and Field 2002; Shreeves et al. 2003; Hatchwell 1999). In wasps, the continuous presence of the breeder on the nest also reduces the chance that the nest will be usurped by nest-less conspecific ‘floaters’. The primary ecological pressures that favor helping in stenogastrines appear to differ qualitatively from those in vertebrates. In many vertebrates, a major ecological constraint on independent reproduction is a shortage of suitable breeding territories (‘habitat saturation’: Komdeur 1992; Pruett-Jones and Lewis 1990; Walters et al. 1992). In contrast, wasps and bees are not territorial. A potentially analogous factor, the cost of nest initiation, while important in at least one extreme environment (McCorquodale 1989), is not enough to alone favor helping in L. flavolineata or an allodapine bee (Bull and Schwarz 1996; Field et al. 1998a). Insurance advantages appear to be a major factor that does favor helping in both stenogastrines and polistines (Reeve and Nonacs 1997; Field et al. 2000; Shreeves et al. 2003). Insurance advantages have not been seriously investigated in vertebrates, but may be less important (but see Langen 2000). One reason is that carer mortality rates in vertebrates are probably lower in relation to the period of offspring dependency than they are in wasps (Queller 1996). For example, Davies (1992) reports that only 13–20% of dunnock breeders die during the breeding season itself. A second reason is that while wasps can potentially recycle excess offspring at minimal cost after the death of a carer, this may not be an option for non-carnivorous vertebrates such as many birds, in which previous investment may be lost after a carer dies (Shreeves et al. 2003). One similarity between cooperatively breeding vertebrates and stenogastrines in particular among wasps may be that resource inheritance is a significant benefit of remaining on the natal nest (as also in termites: Korb, this volume). Two features of stenogastrines underlie this. First, stenogastrine groups are always small, so that helpers may always have a reasonable chance of outliving individuals ahead of them in the queue to inherit (Field et al. 1999; Shreeves and Field 2002). Second, stenogastrine helpers can potentially wait indefinitely for their chance to inherit. This is a consequence of their relatively aseasonal tropical environment, in which

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there is no absolute winter to truncate the lives of individuals waiting in the queue. Whether the chance of inheritance in stenogastrines is quantitatively similar to that in vertebrates remains to be seen, however, particularly given the significantly higher survivorship of the dominant egg-layer compared to her helpers in L. flavolineata (Field et al. 1999; Shreeves and Field 2002). While resource inheritance has long been viewed as a significant benefit for vertebrate helpers, the possible importance of other direct benefits has been emphasized only recently (reviewed by Clutton-Brock 2002). One of these, that by helping an individual may improve its chances of eventually mating with the opposite-sex breeder, does not apply to wasps and bees, where mating occurs outside the group. A second direct benefit, demonstrated in some vertebrates, is that by remaining in its natal group an individual may increase its expected survivorship, perhaps because larger groups are better defended against predators. L. flavolineata is one of the few wasps for which reasonably comprehensive demographic data exist from natural populations. These data suggest that helpers do not have lower mortality rates than independent-nesting females (Field et al. 2000). It would, however, be interesting to compare their mortality rates with those of nest-less floaters, but reliable survivorship data do not currently exist for floaters. Another direct benefit of helping that has recently been highlighted is group augmentation (Kokko et al. 2001). An example is when an individual can boost (augment) group size by helping, so that she will later have more helpers herself if she survives to inherit. By helping, L. flavolineata females do increase the number of offspring reared by the group, and the age-based queuing system ensures that such offspring are indeed potential future helpers themselves. This indicates that group augmentation benefits do exist, but their importance in driving patterns of helping behavior is less clear. Group augmentation effects alone should cause females nearer the front of the queue to work hardest: they have the greatest chance of inheriting and therefore of receiving help from any offspring that they contribute to rearing. That high-ranking helpers in fact work less hard than low rankers suggests that potential group augmentation benefits are outweighed by the negative effect that working harder would have on the chance of inheritance itself (Field et al. 2006). The relative importance of direct versus indirect benefits in driving helping remains an interesting area for future research in L. flavolineata and other insect and vertebrate taxa. In conclusion, although the evolution of helping in both wasps and vertebrates can potentially be understood using the framework provided by Hamilton (1964), the critical ecological factors seem to be fundamentally different in these two major taxa (see also Chap. 7, for a comparison with lower termites). Simply measuring genetic relatedness cannot provide a clear understanding of why helping evolved, or explain individual variation in helping decisions. Costs and benefits are just as important, and the natural history of hover wasps makes them an ideal system for investigating these costs and benefits. Acknowledgments It is a pleasure to thank all those with whom I have collaborated in studying hover wasps, especially Alan Bolton, Cathy Bridge, Mike Cant, Maurizio Casiraghi,

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Adam Cronin, William Foster, Gavin Shreeves and Seirian Sumner. Rosli Hashim and his colleagues at the University of Malaya, Laurence Kirton (FRIM), and K. Durai at WWF Fraser’s Hill, have unfailingly and generously provided facilities and helped with logistics in Malaysia. Judith, Miranda and Lydia Field have all provided essential support and inspiration. I also thank the Natural Environment Research Council for a sustained period of funding. J. Korb and J. Heinze provided constructive comments on the manuscript.

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Chapter 5

Why are so Many Bees but so Few Digger Wasps Social? The Effect of Provisioning Mode and Helper Efficiency on the Distribution of Sociality Among the Apoidea Erhard Strohm(* ü ) and Jürgen Liebig Abstract Sociality has evolved predominantly in a few taxa within the animal kingdom. Even within the Hymenoptera, which are famous for their abundance and diversity of social life forms, eusocial species are very unevenly distributed among different families. Here we ask why within the superfamily Apoidea so few sphecid wasps but so many bees have become eusocial. We argue that the crucial difference between these two taxa is the type of resource provided for the progeny and that this has important consequences for the evolution of sociality. Sphecids provision brood cells with dead or paralyzed arthropods whereas bees gather pollen and nectar as larval food. In social Hymenoptera, workers are often smaller than the foundresses, since this saves some resources in particular at the beginning of the nest founding. However, the large size of the prey of sphecids requires a female to generate a certain minimum amount of power to bring the prey to the nest. Thus, small and/or weak females would not be successful at all and would not represent valuable helpers. In bees, however, small individuals are capable of gathering pollen at a comparatively high rate. Furthermore, the evolution of sociality might be facilitated if foundresses can save investment by providing sexuals and helpers only with the resources that are necessary for their respective task. Such a task-related investment for progeny might be much easier in bees than in sphecids, since the former can provide pollen of different plant species and different proportions of nectar whereas the latter cannot control the quality of the larval food to such an extent. The large size of the prey of sphecids has also enabled a unique strategy of oviposition for larval parasites. Flies and cuckoo wasps might oviposit on the prey while it is carried to the nest by a sphecid female. This “out-of-nest” parasitism cannot be countered by communal nesting, for example, making early steps of sociality less beneficial than in bees where this type of parasitism does not occur. We conclude that one of the most basic ecological features, the type of resource used for provisioning, might have far-reaching consequences for the evolution of sociality in the Hymenoptera.

Erhard Strohm Department of Zoology, University of Regensburg, 93040 Regensburg, Germany [email protected]

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Introduction

The evolution of sociality is still one of the most intriguing problems of evolutionary ecology. Many hypotheses have been put forward to explain the transition from a solitary to a social lifestyle (Wilson 1971, 1975; Choe and Crespi 1997). Hymenoptera play an important role for studying the evolution of sociality due to the multitude of independent origins of sociality and the variation in the complexity of their social organization. Usually, eleven independent cases of the evolution of eusociality among Hymenoptera are assumed (Wilson 1971, 1975). Recent molecular analyses, mainly on halictid bees, indicate a slightly lower number but suggest in the same vein several reversals from sociality to solitary life style, indicating that the transition between the two life styles is more common than previously assumed (Wcislo and Danforth 1997; Danforth 2002). Hamilton (1964, 1972) offered an explanation for the disparity in the distribution of sociality among taxa of insects and argued that the predominant sex determination mechanism, haplodiploidy, might have pre-adapted Hymenoptera for becoming social. While becoming the textbook explanation for the over-representation of sociality in the Hymenoptera, the role of haplodiploidy in the initial steps towards sociality has been increasingly questioned (e.g., Andersson 1984; Bourke and Franks 1995; Choe and Crespi 1997). During the last decades, alternative explanations have been put forward that focus on the ecological conditions that might favor sociality. The obvious approach to analyze, which ecological factors have favored sociality, is to examine the ecological conditions under which primitively social species live or have probably lived during the initial steps towards sociality. The complementary approach -to examine species that are closely related to social ones but did not evolve sociality- has rarely been explored. Here we focus on the case of the sphecid wasps, which are the sister taxon of bees and show a striking similarity in ecological parameters but, in contrast to the latter, have evolved eusociality only once (Matthews 1991; Brockmann 1997). In this chapter we compare ecological conditions between bees and sphecids that might have contributed to the different prevalence of sociality in these taxa. A priori there are two possibilities why an evolutionary step did not happen in one taxon opposed to another: constraints or different payoffs of the initial steps. Therefore, we will consider both, ecological settings that might constrain the evolution of sociality in sphecids and conditions that might make initial steps towards sociality less beneficial in sphecids as opposed to bees. Comparative approaches have frequently been applied to elucidate factors that might promote sociality. Most studies compared aculeate Hymenoptera as a whole with other insects, or with other Hymenoptera (Andersson 1984; Brockmann 1994; Schwarz et al. 1998). The main results of these studies were that both the construction of a nest as a centre of reproductive activities and provisioning of the progeny are important prerequisites for the evolution of sociality (this might not apply to termites, see Chap. 7). In contrast to species that just deposit their eggs somewhere, provisioning or feeding of larvae provides opportunities for alloparental care and a

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nest might be expensive to construct so that it requires many individuals to establish it (Andersson 1984; Ross and Matthews 1991). Nest reuse offers the potential for association of individuals and might, thus, represent an initial step towards nest sharing. Progressive provisioning (i.e., parents continuously provisioning their progeny with food during the larval period) has also been quoted to facilitate the evolution of sociality (Evans 1977). Progressive provisioning certainly represents a derived trait that, in some species, might in fact facilitate the evolution of sociality according to insurance-based models (e.g., Queller 1989, 1994; Gadagkar 1990; Field et al. 2000; Field and Brace 2004; Field 2005). However, the occurrence of many mass provisioning bee species (i.e., parents providing large amounts of food in a brood cell without contact to their progeny) diminishes the importance of progressive provisioning as a general prerequisite for sociality (see also Matthews 1991). Moreover, the frequency of mass provisioning and progressive provisioning does not conspicuously differ between sphecids and bees (in fact, there seem to be more progressively provisioning sphecids). Thus, the mode of provisioning is unlikely to explain the difference in the prevalence of eusocial species. We do not provide an exhaustive analysis of all possible life-history characters and ecological factors and we will only briefly consider the arguments that have already been suggested for the evolution of sociality in sphecids (mainly Matthews 1991; Brockmann 1997), but will focus on certain aspects that have not yet received much attention. We first give a short description of the levels of sociality within the sphecid wasps and bees. Then we present different hypotheses that might help to explain the disparity in eusocial species between the sphecid wasps and the bees. Empirical tests of these hypotheses might provide new insights into the evolution of sociality at least in bees and sphecid wasps.

5.2 5.2.1

Levels of Sociality Sphecid Wasps

Sphecid wasps comprise a paraphyletic group of mostly hunting Hymenoptera (for recent analyses of their phylogeny see Brothers (1999) and Melo (1999) ). Together with the bees (Apidae), sphecid wasps form the superfamily Apoidea. We will use the term sphecid wasps to refer to the members of this superfamily without the bees. It is currently debated which group (family) among the sphecid wasps represents the sister group to the bees. Sphecids comprise about 9000 described species whereas there are about 25,000–30,000 species of bees (e.g., Gauld and Bolton 1996). The majority of sphecid wasps show parental care similar to most solitary bees. Most species mass provision brood cells but there are also species that exhibit progressive provisioning, thus showing extended brood care. Several species,

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mostly from the genus Cerceris, have been reported to exhibit nest sharing (see Table 5.1 in Matthews 1991). In C. antipodes, usually two related females share a nest with the possible benefit of an increased protection against ants, parasites and usurpation by conspecifics (McCorquodale 1989; Brockmann 1997). However, division of labor does not pertain to reproduction in these species. There is only one species of sphecid wasps that has clearly been shown to be eusocial: Microstigmus comes a species belonging to the Pemphredoninae. The genus and in particular the species show some unusual features with regard to nesting behavior. In M. comes, groups of females inhabit self-built nests. They collectively provision brood cells with collembolans and, due to the small size of this prey, one progeny needs more than one hundred prey items for its development to adulthood (Matthews 1991). The question why only this species became eusocial within the sphecids was discussed in detail by Matthews (1991). Briefly, he concluded that several factors might have promoted sociality in M. comes. First, females have to work together to construct the nest because it is made of costly silk, which is much easier to provide collectively. He further suggested that the usage of small abundant prey, which is available throughout the year, the high nestmate relatedness, the long lifespan, as well as the female-biased sex ratio and the delayed production of males might have favored the evolution of eusociality. In contrast, parasitism is infrequent and was therefore not assumed to play an important role as promoter of sociality in M. comes (Matthews 1991). The answer to the question why only M. comes has become eusocial among the sphecid wasps might differ from that why so few sphecids have become eusocial. For example, Matthews (1991) considered the construction of a silk nest in M. comes as most important. However, eusocial bees neither construct silk nests nor do they usually have nests that require collective construction. Thus, these factors cannot explain the disproportionate distribution of eusociality within the Apoidea. Nevertheless, some aspects of the biology of M. comes might be useful for our discussion.

5.2.2

Bees

In bees we find the whole variety of levels of sociality ranging from subsocial, communal, quasisocial, and semisocial to eusocial organization. The number of cases of the evolution of sociality among bees is still under debate but is probably at least about eight times (Danforth 2002; Michener 2000). While stingless bees (Meliponinae) and the honeybees (Apis spp.) show a high level of eusociality with large colony sizes and nests consisting of wax combs located in trees, the majority of the bee species is solitary and nest in the ground (Michener 2000). Some of the groups, mainly the Halictidae, show a striking plasticity in social organization expressing the whole range of sociality (e.g., Wcislo 1997; Miyanaga et al. 1999). In our comparison we mainly focus on ground nesting species of the Halictidae.

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Differences Between Sphecids and Bees

Sphecid wasps and bees have very similar life histories (e.g., Gauld and Bolton 1996). With the exception of parasitic species, all provision brood cells. Most species exhibit mass provisioning but there are also species with progressive provisioning in both groups. Bees and wasps mostly carry their larval provisions to a nest in flight, although there are some species of sphecids that drag their prey over the ground. The nest sites and types of nests are also very similar with most species in both taxa nesting in self constructed subterranean nests, some species nesting in pre-existing cavities aboveground, and a few species constructing brood cells of loam or other material. Both taxa suffer from parasites (kleptoparasites as well as parasitoids) that try to use the provisions for their own reproduction. While the proportion of species that show different modes of provisioning or nesting might differ somewhat between sphecids and bees, there is no obvious pattern with regard to these factors that might explain the discrepancy in the occurrence of eusociality. However, there is one conspicuous difference between the non-parasitic sphecid wasps and bees: the type of resources they use as larval provisions. Whereas all sphecids hunt and paralyze (or kill) different kinds of arthropods, bees rely on pollen and nectar as food for their progeny. We argue that this difference in the type of resource has far-reaching consequences for the evolutionary potential to pass the early steps of sociality. We will explore different corollaries of the resource type and discuss the consequences for the evolution of sociality.

5.3 5.3.1

Body Size and Worker Efficiency Potential for Helping

The size of the resource item used as larval provision by sphecids, namely arthropods, is (mostly) rather large compared to the body size of a species. By contrast, pollen is very small relative to the size of a female bee. Nectar and pollen represent a continuous resource and each forager can decide how much to collect and transport to the nest. Thus, the load can be optimized with regard to flying and carrying abilities. In sphecids, the prey has to be transported to the nest as a whole. This contrasts, for example, with vespid wasps, which chop up large food items into smaller pieces. If the prey of a sphecid wasp is very large and the distance to the nest small, the victim is brought to the nest by dragging it over the ground. If the prey is about the size of a sphecid female or smaller and the distance to the nest is large, then the prey is carried in flight. The number of prey items per brood cell varies considerably, both within and among species (see Tables 3-1 to 3-6 in O’Neill

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2001). In many species, the minimum number of prey items per brood cell is often low (1–4), meaning that the prey is of considerable size compared to the size of the wasp species. Flying with such a comparatively heavy load is a highly demanding activity, since the wasp has to generate enough lift to take off and continue the flight (e.g., Strohm and Linsenmair 1997). Female sphecids often take the largest prey individuals that they can carry in flight (Coelho and Ladage 1999), perhaps to optimize foraging. In some species, such as Sphecius speciosus, flying with heavy prey is only possible by climbing up plants to attain an elevated position for take-off (Coelho 1997). This results in a correlation between a female’s body size and the size of the prey it carries to the nest (Strohm and Linsenmair 1997; Coelho and Ladage 1999). Larger individuals can carry heavier loads in sphecids and there is a critical threshold for the size ratio between carrying wasp and prey below which no prey can be used (Fig. 5.1). More importantly, female size and measures of reproductive success are often strongly positively correlated in sphecid wasps (e.g., Sceliphron assimile (Freeman 1977, 1981; Freeman and Johnston 1978), Cerceris arenaria (Willmer 1985), C. halone (Byers 1978), Palmodes laeviventris (Gwynne and Dodson 1983) and Sphecius grandis (Hastings 1986) ). Although, no size advantage has been found in Bembix rostrata females (Larsson and Tengö 1989), in most sphecid wasps there is a clear advantage of large body size with regard to foraging and thus provisioning success. Across species of bees, the size advantage seems to be less pronounced. Only in two species, Megachile apicalis (Sugiura and Maeta 1989, see also Kim and Thorp 2001) and Osmia cornifrons (Kim 1997), do larger females have a higher reproductive success. In O. cornifrons this is due to a higher rate of brood cell production in large individuals (Kim 1997). No strong effect of female body size

Fig. 5.1 Assumed distribution of the size of a resource item used for provisioning, “Pollen/ Nectar” (dotted line) and “Prey” (dashed line), and the carrying capacity of individuals for “Bees” and “Sphecid wasps”. The continuous lines represent the mean for a species, the grey area the range of the individual capacities from small to large individuals. Small resource items can be carried by all individuals, whereas the probability declines for larger items. Note that small sphecid wasps are hardly able to carry the smallest prey, whereas small bees are able to carry considerable loads of pollen and nectar compared to large individuals

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is apparent in four other megachilids (Tepedino and Torchio 1982; Frohlich and Tepedino 1986; Sugiura 1994; Bosch and Vicens 2006, and references therein) and one anthophorid bee (Johnson 1990). In our own studies we also could not find an advantage for large females in two species of megachilid bees (O. bicornis and O. brevicornis, E. Strohm, H. Daniles, C. Warmers, unpublished). Large females brought more provisions per foraging trip, but had a lower foraging rate. Thus, the relationship between size and foraging efficiency is at least weaker in bees than in sphecid wasps. Since body size largely depends on the amount of larval provisions (Strohm 2000 and references therein), the relationship between parental investment and offspring foraging efficiency should be shallower and the y-intercept (i.e., the amount of provisions necessary for a progeny to have any success) should be at lower values in bees than in sphecids (Fig. 5.1). This has been shown for the sphecid Philanthus triangulum, the European beewolf, where higher investments result in more successful daughters (Strohm and Linsenmair 2000). In this species, at least three prey items are necessary to produce a successful daughter, resulting in a step function of the investment dependence of reproductive success. Why should this be important for the evolution of sociality? The resources for producing offspring are certainly limited. Thus, there is a trade-off between size and number of offspring (Smith and Fretwell 1974; Strohm and Linsenmair 2000). A larger number of smaller offspring might be favorable if the size dependence of progeny success is weak and the whole working potential is less affected by losses due to predation and other causes of mortality. Foundresses of aculeate Hymenoptera have full control over the quantity and quality of provisions that the progeny of their first brood can consume. In fact, in most social bee species, foundresses produce a number of helpers that are smaller than themselves (Anderson 1984; Strohm and Bordon-Hauser 2003). Apparently, this is also the case in the only eusocial sphecid wasp (Matthews 1991). However, the production of small prospective workers only makes sense if their potential value as a helper, i.e., their foraging success, is not affected too much by small size. Since in most sphecid wasps there is a considerable size advantage, small workers would be of no particular help, since they would be much less effective in subduing and carrying prey. A change to smaller prey species might be excluded in most sphecids due to specialization with regard to prey finding and subduing mechanisms. Some species gather prey of different sizes (e.g., Ammophila) and small prey might take less time to be gathered (Field 1992). Still the potential of small individuals to hunt very large, cost-effective prey is probably compromised and their overall hunting success therefore reduced. In bees, however, small workers gather less pollen and nectar per foraging trip but might compensate for this by a higher foraging rate and are nearly as good as larger individuals. Therefore, the value of small workers could be much greater in bees compared to wasps. Remarkably, the sphecid wasps that have the most highly evolved levels of sociality hunt on very small prey (Microstigmus on collembolans, Spilomena on thrips, Matthews 1991; Melo 1999). In Microstigmus comes the collembolans are “packed into a compact ball” (Matthews 1991, p. 590) and the egg is deposited on the prey ball, similar as in bees that oviposit on the pollen ball. Matthews (1991)

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already pointed out that stocking brood cells with multiple small prey might represent a good opportunity for helping, since “Rapid collection of small prey can be shared easily among several females, whereas a single female would not only require an inordinately long time to collect the equivalent amount, but would incur the additional costs of an extended period of nest vulnerability….” (Matthews 1991, p 590). The collembolan prey is abundant and it does not require large powerful hunters to overwhelm it and bring it to the nest. Provisioning a brood cell by a single female would take too long and would most probably result in parasitism (see Goodell 2003) or a highly increased risk of microbial degradation of the prey (see Strohm and Linsenmair 2001). Thus, the size of the resources that serve as larval provisions relative to the size of the forager might have important implications for whether a worker can provide valuable help or not. Not surprisingly, a similar trend can be seen in the vespid wasps. There are many species of eumenids that provision brood cells with entire paralyzed arthropods like sphecids; whereas the polistine, vespine and stenogastrine wasps chop their prey up before they transport it to the nest. In line with our hypothesis there are many eusocial polistine, vespine and stenogastrine wasps whereas there is no known eusocial species of eumenids (Ross and Matthews 1991). Thus, the superfamily Vespoidea provides an independent lineage with similar relationships between the size of items for provisioning larvae and the distribution of sociality as the superfamily Apoidea.

5.3.2

Parental Investment and Progeny “Quality”

The limitation of resources for reproduction might have further, more intricate, implications for the evolution of sociality. Craig (1983) as well as West-Eberhard (1975) already pointed to the importance of helper efficiency. Here we argue that one precondition for the evolution of eusociality may be that there are differences between a reproductive and its helper(s) in their ability to reproduce. However in contrast to Craig (1983), we do not focus on fertility (i.e., the ability to lay eggs), but on the entire set of abilities necessary for successful reproduction and on the quantity and quality of parental investment that is needed to attain this full potential as a reproductive. Although the scenario is largely speculative at the moment, it might stimulate the integration of an ecological background and, thus, broaden the view on the evolution of sociality. If reproductives and helpers are equally capable of producing offspring, reproductive division of labor is only beneficial if additional emergent properties of the cooperation per se exist. Such emergent benefits are not needed if there are inequalities between reproductives and helpers because of the following. Assume that the reproductive abilities of individuals can be divided into two components; first there is the ability to found a nest, i.e., to successfully go through all stages from mating, overwintering (only in temperate regions), dispersal, nest finding, nest construction and oviposition. The second component is the ability to forage

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for provisions and raise offspring. Whereas solitary individuals or foundresses have to perform both components, only the second part, the ability to gather resources, is needed by helpers. These two abilities might be partly independent of each other and they might depend on quantitative or qualitative features of the resources provided by the mother (Fig. 5.1). Assuming such conditions, a foundress would have the opportunity to provide a progeny ‘only’ with the resources that are necessary for its ability to forage, but save the additional investment that would be necessary to provide a progeny with the ability for nest founding (Fig. 5.1). The amount of investment saved increases with the amount of investment needed for a progeny to obtain founding abilities. The possible benefits of saving resources will of course increase with increasing resource limitation. Such limitations might be exaggerated by temporal or spatial fluctuations or population density (e.g., in halictid bees: Richards and Packer 1996, 1995). If a reproductive produced offspring with reduced abilities to reproduce directly but a high efficiency of helping, one would expect that this strategy becomes fixed in analogy to what Craig’s subfertility model suggests (Craig 1983), given the production of helpers is beneficial at all. While Craig focused on the reduced egg laying ability of the helper, we think this might be misleading, since producing an egg is probably cheap compared to the other components of parental investment needed to produce offspring. In Polistes dominulus, for example, foundresses are capable of triplicating their egg-laying rates above the average without getting depleted of eggs for an experimental period of 2 weeks (Liebig et al. 2005) indicating that the production of eggs is not too expensive. In addition, with the exception of a very small number of ants, helpers in almost all hymenopteran societies have retained the ability to lay reproductive eggs (e.g., Wilson 1971; Hölldobler and Wilson 1990) and do so at least in orphaned colonies (e.g., Bourke 1988). For example, in a stenogastrine wasp, such helpers were able to become reproductives when they no longer had to invest in nest construction (Field and Foster 1999). Thus, fertility is not the limiting factor to become a successful reproductive; rather, the ability to successfully reach the stage where the first eggs are laid, besides the subsequent investment in successful offspring rearing is key to successful reproduction. Focusing on the two components of reproduction, founding and helping, allows one to link the subfertility hypothesis to the headstart or insurance hypothesis (Queller 1989, 1994; Gadagkar 1990). These hypotheses assume that helpers do better in raising siblings than own offspring when the mortality regimes differ between both situations. This is the case when founding a nest is costly and mortality is increased until the first eggs can be laid. Successful nest founding may depend on the quality of the foundresses that can possibly only be obtained by an optimal supply with resources during the larval stage. Individuals that experience suboptimal larval conditions fare better by helping, since this reduces their mortality. Moreover, under these conditions, the helper’s mother saves the additional futile investment required for producing successful foundresses with the consequence that the inclusive fitness of both foundress and helper are maximized.

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Our hypothesis, of course, depends on the validity of the assumptions. Species in which investment in founding and helping abilities can be separated might be able to produce effective helpers that would, however, fail to found a nest. Yet, such a demand-oriented allocation of parental investment is not possible in species in which helper and founding abilities are closely coupled. Under poor conditions they will produce low-quality offspring that are neither good in founding a nest nor in helping to raise siblings. As already outlined, sphecids usually use comparatively large prey as larval provisions which requires a certain body size to efficiently carry the prey back to the nest. As smaller individuals are less and less capable of prey transportation, their relative efficiency declines with body size. Thus, in sphecids, foraging efficiency might be closely linked to the overall quality of an individual and a reduction in the amount of resources might result in individuals that are too small to be of use as a helper. Actually, the quality, i.e., nutrient composition and content of trace elements, might be even more important than the quantity. Sphecid mothers might have little opportunity of manipulating the quality of the provisions since the composition of the food items can hardly be controlled. Thus, it would be difficult for a sphecid mother to save parental investment by providing a progeny with the quantity and quality of provisions that is just sufficient to become an efficient helper (Fig. 5.1). The situation is different in bees. As bees can carry small pollen loads, the relative efficiency does not decline so much with decreasing body size, as discussed above. Thus, bees can possibly reduce the amount of provisions without disproportional decreases in the foraging efficiency of their progeny. Moreover, bees provide their progeny with pollen and nectar of different plant species. The composition of pollen, in particular their protein content, differs between different plant species (Roulston and Cane 2000, 2002). Mother bees could, thus, provide their progeny with pollen of different quality and could vary the proportion of nectar among brood cell. Thus, bees have much more opportunities to control the quantity and quality of their larval provisions. With regard to our scenario, helper and foundress abilities might be (at least partly) under control of the foundress in bees, which allows the saving of investment in nest founding abilities of its first offspring (Fig. 5.1).

5.3.3

Evidence

The presence of variation in size and quality that predisposes individuals for either reproductive or helper roles has been identified repeatedly throughout the social Hymenoptera (e.g., Crespi and Choe 1997). However, we do not want to repeat the importance of specialization as a factor in the evolution of sociality but highlight the conditions that allow for the separation of reproductive tasks and possibly further specialization in insect societies.

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Such variability in capabilities and specialization occurs at different levels of expression. A weak differentiation of abilities was found in paper wasps. In Ropalidia marginata co-foundresses in a foundress association have a lower reproductive success in comparison to the dominant female when forced to nest alone in the field (Shakarad and Gadagkar 1997). Co-foundresses may thus decide to join a foundress association on the basis of their rearing abilities. Usually, however, the differences in abilities are expressed between foundresses and helpers. In Polistes wasps, the foundress is usually larger or of higher quality than its helping workers from the first generation, although foundresses and workers often do not differ in morphology (Solís and Strassmann 1990; Reeve et al. 1998). Similar differences between the first helper brood and the later brood that represents the foundresses of the next year are known from Bombus (e.g., Knee and Medler 1965). In halictid bees there is differential provisioning of workers and female sexuals (Richards and Packer 1994): provisions in queen-destined brood cells are larger and contain more sugar. This has the effect of larger fat reserves in prospective queens that enable them to hibernate. Such increased fat reserves in prospective foundresses can be found in several species of halictid bees (e.g., Richards and Packer 1994; Strohm and Bordon-Hauser 2003). Within the framework of our scenario such fat reserves might represent an example for the component that is necessary for nest founding, whereas it seems to be dispensable for foraging. The fat reserves serve as energy stores for hibernation (e.g., Beekman et al. 1998) and possibly nest founding (Weißel et al. unpublished). This kind of differential investment in sexuals and workers as adaptation to founding and helper tasks is well known from more derived groups. Here, specialized castes are determined by differential feeding in certain stages of larval development (Wheeler 1986). In the Hymenoptera, the most pronounced differences between the foundresses and their offspring are found in ants (Chap. 6). The ancestral situation is that a morphologically distinct queen founds a colony and her offspring, the workers, care for the brood (e.g., Hölldobler and Wilson 1990). If queens found their colonies independently, i.e., without the help of others, they contain more energy reserves and are larger in comparison to species in which queens found colonies dependently, i.e., with the help of workers (Keller and Passera 1989; Stille 1996). This pattern indicates that nest founding is an extremely difficult task and requires a large proportion of the reserves. In ponerine ants, for example, the dimorphism between the queen and workers is less pronounced than in most other ant subfamilies (Peeters and Ito 2001). Despite the reproductive degeneration of workers in most ant species, many ponerine species have workers that are reproductively fully competent. Nevertheless, neither in this nor in other ant subfamilies do workers occur that are able to found colonies in the field, although they are capable of doing so under laboratory conditions (Liebig et al. 1998). This indicates that the worker morph is specialized on helper tasks but no longer sufficiently successful in solitarily performing the whole repertoire of tasks necessary to reproduce on their own. Even though ponerine ants are predators, they differ from sphecid

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wasps as they are not specialized but usually prey on a large variety of differently sized soft-scaled arthropods. Thus, differences in size are not as important in ponerines for foraging efficiency as in sphecids.

5.4

Parasitism

5.4.1

Defense Against Predators and Parasites

Nests of aculeate Hymenoptera contain brood cells stocked with highly nutritive provisions that are most attractive to a variety of kleptoparasites and brood parasitoids (e.g., Evans and O’Neill 1988; Wcislo and Cane 1996). These can cause a high rate of brood cell failure. Here, we distinguish different types of parasites because this might have implications for the benefits that could be obtained during the initial steps towards sociality, like communal nesting. One could define four main types of organisms that can be regarded as brood parasites in a broad sense: pathogens, microbial competitors, brood cell parasites, and “Trojan horse” parasites. The latter term refers to the fact that these parasites oviposit or larviposit on the prey and their eggs or larvae are carried into the brood cell by their host; thus, the prey functions as a Trojan horse. See Table 5.1 for characteristics of these types of brood parasites.

Table 5.1 Classification of parasitization in bees and sphecids Type of parasite Mode of parasitism Organisms (References) Pathogens Microbial competitors

Brood cell parasites

“Trojan horse” parasites

Infection of larvae from mother, provisions or from nest. Infestation of provisions from mother, provisions or from nest. Consumption or contamination of provision causing food reduction and /or intoxication, possibly starvation of larvae. Oviposition in brood cell or in nest, either parasitoid or cleptoparasitic. Deposition of eggs on prey, e.g., during nest approach of the provisioning individual, either parasitoid or kleptoparasitic

Mostly fungi, bacteria, probably viruses (Torchio 1992) E.g., mould fungi (Strohm and Linsenmair 2001)

Several arthropods, e.g., Sapygidae, Chrysididae, Mutillidae (Evans and O’Neill 1988) Satellite flies, some Chrysididae (e.g., Strohm et al. 2001, Spofford and Kurczewski 1992)

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Nest Aggregations

Parasites have frequently been proposed to favor sociality (Lin and Michener 1972) through the selfish herd effect (e.g., Wcislo 1984; Rosenheim 1990; see also Chap. 9). If the risk of being parasitized is reduced in a dense group of conspecifics, aggregated nesting might reduce failure due to parasitism. Nest aggregations might be effective against brood cell parasites and “Trojan horse” parasites, since these might be driven away (Matthews 1991) or confused by the high density of host nests. By contrast, the impact of pathogens or microbial competitors is unlikely to be reduced by nest aggregations. Dense aggregations might even enhance the chances of infection and infestation (Schmid-Hempel 1998). The aggregation is thought to result in increased social contact that might facilitate the evolution of sharing of nest entrances or entire nests. This nest aggregation hypothesis requires that the rate of parasitism is negatively density-dependent. However, negative density dependence was not the rule in the respective studies (Rosenheim 1990; Molumby 1995; Strohm et al. 2001). No density-dependence or positive density dependence was also frequently observed. The latter would even select for dispersed nesting. If parasitism is more often negatively density-dependent in bees than in sphecids this could select for more aggregated nesting and facilitated nest sharing. Such differences in density-dependence might result from differences, among other things, in nest sites, in the predominant provisioning behavior, in the predominant type of nest parasite, and in the possible mechanisms of nest defense. The available data do not allow such an analysis at the moment. However, considering the consequences of prey size for the benefits of aggregated nesting might be fruitful. First, the size of the prey of sphecids enables “Trojan horse” parasites to deposit eggs on the prey during the approach or entering phase. This has been described for brood parasites of several sphecid wasps, such as chrysidids (Veenendaal 1987) and in certain kleptoparasitic, so-called satellite flies that pursuit prey-laden females and deposit larvae on the prey before the female enters the nest (Spofford and Kurczewski 1992, O’Neill 2001, E. Strohm unpublished). Bees, in turn, carry pollen that does not allow a parasite to deposit an egg on it. Second, in sphecids the flight performance of homing females might be heavily compromised by the comparatively large size and mass of the prey. Therefore, the approach and entering of the nest might require longer and evasive flights (Spofford and Kurczewski 1992) may be less effective or require more energy than in bees that carry comparatively smaller loads. These factors favor brood parasites, which wait in the nest area for homing prey-laden hosts and try ovipositing on the prey. The probability for successful parasite oviposition will probably increase with the number of host nests within the detection area of the parasite. Therefore, parasites will accumulate in nest aggregations of their hosts. The resulting density dependence will probably be

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positive. Thus, the mere fact that bees gather small particles as provisions whereas sphecid wasps carry large prey items predisposes the latter to suffer an additional kind of threat by “Trojan horse” parasites and this threat is likely to be positively density dependent and, thus, selects for dispersed nesting that reduces the potential for social interactions.

5.4.3

Nest Defense

A second important factor favoring the initial steps of sociality might result from sharing of nest entrances or whole nests because of limited nesting space. Limitation of suitable nest substrate has been reported (McCorquodale 1989; Banschbach and Herbers 1996; Potts and Willmer 1997, 1998) or can be implied (Strohm et al. 2001) for several species of solitary aculeates. If two or more individuals use the same entrance, the nest will be left unattended for a shorter period and parasites will have less opportunity to enter a nest unnoticed (Soucy et al. 2003). This might result in a reduced risk of parasitism. Nest defense would definitely help against brood cell parasites, since these have to enter the nest to oviposit. In a next evolutionary step, individuals might guard the entrance for some time, thus further reducing the accessibility of the nest for brood cell parasites (Lin and Michener 1972; Alexander 1974; Abrams and Eickwort 1981). It will, however, not be effective against “Trojan horse” parasites, since oviposition takes place outside of the nest. There will also be no advantage of nest defense with regard to pathogens or microbial competitors. Several authors proposed that nest guarding is one of the most important initial steps towards cooperation between individuals in bees (e.g., Schwarz et al. 1998). However, if the largest proportion of parasitism happens by “Trojan horse” parasites outside the nest, selection for guarding will not be as strong. The predominant brood parasite of the European beewolf, the chrysidid wasp H. rutilans is even able of altering its mode of egg deposition. It either oviposits on paralyzed honeybees, which are stored in the main burrow (brood cell parasite), or tries to attach to the bee and oviposits while a female enters the nest (“Trojan horse” parasite, Strohm et al. 2001). Thus, these chrysidids can adjust their strategy depending on the conditions. Guarding of the nest would, in this case, be not very helpful. The distribution of lower levels of sociality, communal, quasisocial and semisocial lifestyle, among sphecids and bees supports this pattern. There are very few documented cases of nest sharing in sphecid wasps, most of which are in the genus Cerceris (e.g., Alcock 1975; McCorquodale 1989). On the other hand, communal, quasisocial and semisocial species can frequently be found among the bees (Michener 2000). Our classification of parasitism suggests that bees might benefit more from sharing nests since this is effective against brood parasites whereas sphecid wasps do not have this advantage. Parasitism in the form of brood cell parasites as opposed to “Trojan horse” parasites may thus be a factor that promotes initial steps towards sociality in bees.

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Conclusions

Bees and sphecid wasps are phylogenetically closely related and share most of their life-history characteristics. Therefore it is surprising that there are so many independent steps toward eusociality in bees, but so few sphecids have become eusocial. We hypothesized that the basic difference between bees and sphecid wasps, the type of larval provisions, might have had crucial consequences for the evolution of sociality. The large prey of sphecids results in a close relationship between body size and reproductive success. Therefore, small workers would be of no particular help. This is different in bees. Pollen allows being collected in small packages adjusted to the body size of the foraging individual. Thus, a reduced body size does not necessarily change the efficiency of a bee. Assuming that the resources for reproduction are limited, a mother might spare investment by producing helpers that lack the ability to found a nest on their own. This would require that the founding and provisioning abilities can be separated. Such a possibility is less likely in sphecids, because the large prey does not allow mother sphecids to finely adjust the quantity and quality of provisions with regard to the prospective reproductive potential of their progeny. Bees, by contrast, have much more opportunity to provide their progeny with a specific diet that might predispose their progeny to become helpers. The type of provision can thus influence whether cheap helpers are efficient in provisioning that allows them to gain indirect fitness benefits. The type of provision seems also important with regard to brood parasitism and whether social behavior might help to reduce it. In contrast to bees, the use of large prey in sphecids allows for “Trojan horse” parasites. With this kind of parasitism, nest sharing does not provide a particular advantage, which is the case for other forms of brood parasitism. The use of pollen packages precludes “Trojan horse” parasitism, which allows for efficient guarding in shared nests, which may explain some of the variation in sociality among bees. Which of these factors has the strongest effect cannot be decided with the available data. Much more information is needed. First, the size dependence of the foraging success of bees and sphecid wasps and the underlying mechanisms should be investigated to evaluate our hypothesis that small body size is much more disadvantageous in wasps than in bees. Second, the physiological differences between foundresses and helpers and the composition of the respective provisions should be analyzed in detail to test the validity of the assumption that foundresses can save investment by producing progeny that are able to forage but are not able to found a nest on their own. Third, the prevalent parasites of the different groups of bees and wasps and the rate of parasitism should be determined for a reasonable number of representative species and it should be analyzed whether initial steps towards sociality might be effective in reducing these threats. A further extension of this view is the transfer on other animal groups. Is the evolution of efficient cheap helpers possible in vertebrates or is this precluded by life-histories and patterns of provisioning that differ from insects? Possibly,

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physiological constraints only allow the limited specialization in reproductive roles as in the naked mole-rat. Are there any types of parasitism in vertebrates that helpers can efficiently prevent? The comparison of species groups allows identifying potential key factors for the evolution of sociality. We think that the type of resource used for reproduction is such a key factor that strongly affects a species’ potential to evolve sociality. Focusing on resource use might be a fruitful way of further exploring the distribution and evolution of sociality.

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Strohm E (2000) Factors affecting body size and fat content in a digger wasp. Oecologia 123:184–191 Strohm E, Linsenmair KE (1997) Female size affects provisioning and sex allocation in a digger wasp. Anim Behav 54:23–34 Strohm E, Linsenmair KE (2000) Allocation of parental investment among individual progeny in the European beewolf Philanthus triangulum F. (Hymenoptera, Sphecidae). Biol J Linn Soc 69:173–192 Strohm E, Linsenmair KE (2001) Females of the European beewolf preserve their honeybee prey against competing fungi. Ecol Entomol 26:198–203 Strohm E, Bordon-Hauser A (2003) Advantages and disadvantages of large colony size in a halictid bee—the queen’s perspective. Behav Ecol 14:546–553 Strohm E, Laurien-Kehnen C, Bordon S (2001) Escape from parasitism: spatial and temporal strategies of a sphecid wasp against a specialised cuckoo wasp. Oecologia 129:50–57 Sugiura N (1994) Parental investment and offspring sex ratio in a solitary bee, Anthidium septemspinosum Lepeletier (Hymenoptera: Megachilidae). J Ethol 12:131–139 Sugiura N, Maeta Y (1989) Parental investment and offspring sex ratio in a solitary mason bee, Osmia cornifromns (Radzowski) (Hymenoptera, Megachilidae). Jpn J Ent 57:861–875 Tepedino VJ, Torchio PF (1982) Phenotypic variability in nesting success among Osmia lignaria propinqua females in a glasshouse environment (Hymenoptera: Megachilidae). Ecol Entomol 7:453–462 Torchio PF (1992) Effects of spore dosage and temperature on pathogenic expression of chalkbrood syndrome caused by Ascosphaere torchioi within larvae of Osmia lignaria propinqua (Hymenoptera: Megachilidae). Env Entomol 21:1086–1091 Veenendaal RL (1987) The hidden egg of Hedychrum rutilans (Hym.: Chrysididae). Entomol Ber 47:169–171 Wcislo WT (1984) Gregarious nesting of a digger wasp as a “selfish herd” response to a parasitic fly (Hymenoptera: Sphecidae; Diptera: Sacrophagidae). Behav Ecol Sociobiol 15:157–160 Wcislo WT (1997) Behavioral environments of sweat bees (Halictinae) in relation to variability in social oprganization. In: Choe JC, Crespi BJ (eds) Social behavior in insects and arachnids. Cambridge University Press, Cambridge Wcislo WT, Cane JH (1996) Floral resource utilization by solitary bees (Hymenoptera: Apoidea) and exploitation of their stored foods by natural enemies. Annu Rev Entomol 41:257–286 Wcislo WT, Danforth BN (1997) Secondarily solitary: the evolutionary loss of social behavior. TREE 12:468–474 West-Eberhard MJ (1975) The evolution of social behavior by kin selection. Q Rev Biol 50:1–33 Wheeler DE (1986) Developmental and physiological determinants of caste in social Hymenoptera: Evolutionary implications. Am Nat 128:13–34 Willmer PG (1985) Size effects and hygrothermal balance and foraging patterns of a sphecid wasp, Cerceris arenaria. Ecol Entomol 10:469–479 Wilson EO (1971) The insect societies. Harvard University Press, Cambridge Wilson EO (1975) Sociobiology, the new synthesis. Harvard University Press, Cambridge

Chapter 6

Social Plasticity: Ecology, Genetics, and the Structure of Ant Societies Jürgen Heinze

Abstract The close kinship between helping workers and their sexual sisters in haplodiploid Hymenoptera is thought to have favored the evolution of sterile worker castes and altruistic behavior in ants, bees, and wasps. Much research has therefore concentrated on elucidating the genetic structure of Hymenopteran societies. However, variation in kinship appears to be surprisingly unimportant in shaping some of the details of the social structure of insect societies. Instead, major features of the colony phenotype, such as worker number, queen number, reproductive skew, worker policing, and the pattern of allocation of resources towards colony growth or reproduction are more strongly affected by variation in ecological parameters, such as the availability of suitable nest sites for colony founding, resource abundance and the occurrence of social parasites.

6.1

Social Plasticity

Insect societies can be considered as the extended phenotypes of their constituent individuals, and many characters of the society, such as colony size, colony age at maturity, or the allocation of resources to reproduction and colony maintenance, are shaped by natural selection. Most colony-level traits vary enormously between species. In ants, colony size varies over eight powers of ten, from less than 10 in Thaumatomyrmex (Jahyny et al. 2002) to several million individuals in driver ants and Formica supercolonies (Higashi and Yamauchi, 1979). Age at maturity ranges from a few months in colonies that undergo budding to many years in colonies of some monogynous species (Keller and Genoud 1997). Propagule size and the pattern of reproductive allocation (i.e., allocation of resources towards reproduction

Jürgen Heinze Department Biology I, University of Regensburg, 93040 Regensburg, Germany [email protected]

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vs. growth and maintenance) show similar variation. Smaller, but still impressive variation also exists within species, in particular concerning sex allocation ratios, the partitioning of reproduction among inseminated females, queen number and mating frequency, but also colony size and the degree of caste dimorphism (Bourke and Franks 1995; Crozier and Pamilo 1996). In general, such “social plasticity”, i.e., the intraspecific variation of the colony phenotype, might be caused by variation in environmental conditions, different genotypes, or genotype-environment interactions. The fundamental importance of genetic relatedness in inclusive fitness theory (Hamilton 1964) together with the availability of molecular markers for the exact determination of kinship in the field has resulted in a focus of empirical and theoretical efforts to understand the interrelations between the genetic structure and the phenotype of insect societies. Thanks to these studies we know that, with a few exceptions, insect societies consist of families, in which non-zero relatedness is maintained by fencing off alien intruders and through the more or less regular occurrence of nest founding by single queens. In addition, it has become clear that each feature of the social structure that has an impact on the direct or indirect fitness components of individual group members may be sensitive to changes in the genetic structure of the society. Particularly research on sex ratios has highlighted the significance of genetic variation for reproductive decisions (reviewed by Bourke and Franks 1995; Crozier and Pamilo 1996; Mehdiabadi et al. 2003). Furthermore, genetic studies have documented that lineages of workers in genetically heterogeneous societies, such as those of honeybees, may specialize for different tasks (Page and Robinson 1990) and that the social structure (i.e., queen number) of fire ant colonies is determined by different alleles at a certain locus, which apparently codes for a protein involved in queen– worker communication (Ross and Keller 1988; Krieger and Ross 2002, 2005). These and other findings have clearly documented that strong interrelations of genotype and social phenotype exist and have thus prepared the successful advance of sociogenetics and sociogenomics (Breed 1989; Robinson 1999; Robinson et al. 2005; Rüppell et al. 2004). Nevertheless, considerations of kin structure and genes alone are often not sufficient to explain the social phenotype and its inter- and intraspecific variation. In fact, many features of insect societies appear to be remarkably robust against variation in genetic colony structure. For example, whether worker reproduction occurs or not appears to be much less influenced by relatedness than predicted by theory (Hammond and Keller 2004; Korb and Heinze 2004; Heinze 2004; but see Wenseleers and Ratnieks 2006) and several recent studies have documented sex ratio specializations without the expected underlying variability in relatedness asymmetries (Foitzik and Heinze 2000; Brown and Keller 2000; Fournier et al. 2003). Instead, variation in environmental factors, such as climate, resource availability, the occurrence of competitors, predators, or parasites, etc., appears to be as influential as variation of genetic composition at least for some features of the insect society (Nonacs 1986; Hölldobler and Wilson 1990; Herbers 1993; Keller 1995; Hammond and Keller 2004). The importance of ecology in social evolution is clearly emphasized by factors b and c in Hamilton’s rule, i.e., the benefits and costs

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of helping, and numerous researchers have investigated ecological influences on the social phenotype (reviewed by Hölldobler and Wilson 1990). However, the magnitude of environmental constraints is often difficult to measure and many hypotheses about the interrelations of the social phenotype and the environment are therefore not strongly supported by empirical data. Compared to the well-advanced state of population and socio-genetic research on insect societies, socio-ecology therefore lags behind in accuracy and transparency, and many claims about how the environment shapes the social phenotype still remain correlative and need to be tested by long-term manipulations in the field. Nevertheless, the literature teems with an enormous number of examples for either suggested or firmly proven influences of ecological variation on the colony phenotype. Instead of giving a complete review of all these studies, my aim is to summarize for non-specialists what is currently known on the ecology of social evolution particular of ants and to point out some open questions that deserve more attention in the future.

6.2

The Number of Female Reproductives

Variation in the number of queens has long been singled out as one of the most important traits in ant evolution (Buschinger 1968; Hölldobler and Wilson 1977; Keller 1993). Through its impact on average nestmate relatedness and relatedness asymmetries (i.e., the differential relatedness of workers to female versus male sexuals, e.g., Bourke and Franks 1995), variation in queen number plays a major role in inclusive fitness models on sex allocation and has therefore found considerable attention by researchers. Numerous investigations have aimed at clarifying why queen numbers vary between species, and the results of such studies are presumably also of relevance for intraspecific variation. In some rare cases, multi-queen societies arise from cooperative colony founding by several queens (primary polygyny). More commonly they originate from the adoption of young queens by established nests, usually those of their mothers (secondary polygyny). In the second process, queen number is intricately linked with colony founding strategies (e.g., Rosengren and Pamilo 1983; Rosengren et al. 1993). New colonies in obligatorily monogynous species (i.e., colonies have always a single queen) are typically founded independently by solitary queens after some sort of a dispersal and mating flight. In contrast, queens in facultatively polygynous species mostly mate in or near their maternal nests and new colonies may be founded in a dependent way through the fragmentation or budding of established colonies with multiple queens. Alternative mating and founding tactics are often associated with morphological specializations of queens. While most queens that found solitarily have a bulky thorax and are well-equipped with body reserves, queens of polygynous species are often smaller and also lack the fat reserves needed for the independent initiation of a new colony (Keller and Passera 1989; Stille 1996). Queen size and morphology frequently vary also within species (Buschinger and Heinze 1992; Rüppell and Heinze 1999; Heinze and Keller 2000).

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In many cases, the presumed correlation of founding tactics and queen morphology has been indirectly inferred from the association of queen size and queen numbers. Direct evidence exists for Myrmica ruginodis (Brian and Brian 1955) and also for Temnothorax rugatulus, where large queens were significantly more likely to be trapped in the field than small queens (Rüppell et al. 2001a). Ecological factors might affect colony founding and queen number in manifold ways. Hölldobler and Wilson (1977) suggested that polygynous colonies can more easily monopolize habitat patches through building subsidiary nests nearby, and that polygynous species are forced to move frequently between nesting sites because of unstable environmental conditions and therefore have a lower risk of losing their reproductives than monogynous species. In such unstable habitats, early reproduction is generally favored when population sizes increase (Tsuji and Tsuji 1996). Species with independently founding queens have a much longer generation time than species, in which new nests are founded by young queens together with workers from their maternal nest. The advantage of early reproduction in expanding, age-structured populations, might readily explain the success of polygynous species in disturbed habitats (Tsuji and Tsuji 1996; Tsuji 2006). Other studies have highlighted environmental constraints on solitary founding. Wherever the survival rate of solitarily nesting queens is low, selection favors alternative ways of colony founding (Herbers 1993). For example, there is a strong association between the occurrence of polygynous species and latitude. The proportion of Scandinavian ants in which young queens are adopted increases from below 50% in Denmark to above 90% close to the North Cape (Johnsen 1994). Most ant species near the tundra-taiga ecotone and also near the tree-line in alpine areas are indeed facultatively polygynous or social parasites, whose queens invade already established colonies of related species and therefore avoid solitary founding (Heinze 1993; Johnsen 1994). One notable exception are species of the genus Camponotus, but here young queens hibernate in the nest before mating in early summer and therefore have a much longer time available for successfully starting their own nests before the next winter than other ants, whose sexuals usually eclose and mate later in summer (Heinze 1993; Heinze and Hölldobler 1994). It is understandable that solitary queens who are forced to forage during colony founding are exposed to a high predation risk, but why should “claustral” founding, in which queens have enough body reserves to remain sealed in their nests until their first offspring workers eclose, be more costly in boreal than temperate habitats? Workers of Leptothorax canadensis had a lower survival rate when hibernating in isolation in the laboratory than when they were housed with several other workers (Heinze et al. 1996). At present it is not yet clear whether this holds for founding queens, too, but it appears to be safe to assume that the prolonged phase of solitary founding in habitats with long and severe winters is more costly than hibernation in milder environments. A similar but less pronounced trend seems to exist in ants living in desert and steppe habitats. Data on queen number are not available from all of these species, but from the morphology of queens, which often show signs of wing reduction and the loss of long-distance dispersal, it was concluded that new colonies are frequently initiated through budding or colony

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fragmentation also in these areas (Briese 1983; Bolton 1986; Tinaut and Heinze 1992; Tinaut and Ruano 1992). Though average queen numbers may vary strongly between populations of the same species (e.g., Elmes and Petal 1990; Elmes and Keller 1993; Herbers 1986; Ross et al. 1996; Seppä et al. 2004), the evidence for an influence of climate on this intraspecific variation is still not very convincing, perhaps because queen number is usually affected by numerous ecological factors at the same time. The most prominent among these is probably habitat saturation, i.e., the availability of nest sites. This seems particular important in species that live in preformed cavities in wood, such as rotting branches, hollow nuts, or under bark (Herbers 1986, 1993), but has also been demonstrated to affect queen number in soil-nesting species and other ants (Elmes 1980; Pedersen and Boomsma 1999). When such nest sites are (temporarily) limited, young queens may favor returning to their maternal nest over the risk of remaining without a suitable nest site. New colonies may be founded by colony fragmentation or budding once new nest sites have become available, for example, after winter storms have shaken down hollow branches or acorns from trees. In some populations of Temnothorax longispinosus, experimental seeding of habitats with artificial nest sites indeed led to a reduction in average queen number per nest due to the fragmentation of polygynous colonies (Herbers 1986; Foitzik et al. 2004), but not so in Myrmica punctiventris (Herbers and Banschbach 1999). In a study on ants in successional taiga forests, habitat patch age was found to be associated with queen number, probably again because of different nest-site availability and different predation rates (Seppä et al. 1995). A progressive increase of queen number with habitat age has also been documented in the African plant ant Petalomyrmex phylax, though here geographical variation in the social structure of colonies appeared not be associated with variation in nest site availability (Dalecky et al. 2005, 2007). Nest site limitation in densely populated areas appears also to affect colony structure in obligatorily monogynous ants. Some nest sites inhabited by Temnothorax nylanderi, such as hollow acorns and grass stems, are fragile and decay within a few weeks. Towards the end of summer, many established colonies are therefore forced to hunt for a new nest and thus may move in with other colonies if an empty, suitable site is not available. Similarly, young founding queens may seek adoption into alien colonies when they do not find a suitable nesting site (Foitzik and Heinze 1998, 2000, 2001; Foitzik et al. 2003). Both colony fusion and adoption result in the temporary presence of two, typically unrelated queens per nest. However, monogyny is quickly restored by aggression between the queens (Strätz et al. 2002). The frequency of genetically mixed colonies increases with colony density (M. Strätz, unpublished; Fig. 6.1). At present, it is unclear how strongly predation or parasitism might affect queen number. Predation during the colony founding phase, in particular intraspecific brood raids, have been recognized as one of the major selective forces favoring cooperative colony founding in some desert ants (Bartz and Hölldobler 1982; Rissing and Pollock 1987). Similarly, the selection pressure exerted by slavemaking ants might favor multiple-queening. Queens of slave-making ants usurp the

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Fig. 6.1 Percentage of genetically homogeneous colonies and nestmate relatedness (± standard error) in four Central European populations of the monogynous, monandrous ant Temnothorax nylanderi with different nest densities. In dense populations, colonies may fuse, resulting in genetically mixed colonies with considerably lowered relatedness. Numbers above bars indicate sample size (number of colonies)

nests of related species, kill or expel the resident queens, and take possession of the present brood. The workers that eclose from the conquered brood serve as slaves, i.e., they forage for food and nurse the parasite queen’s young. Slave-maker workers eventually pillage new slave worker pupae from neighboring host nests to replenish the workforce in their own nest. Both, usurpation and slave-raids, may have a strong influence on queen number in host colonies (D’Ettorre and Heinze 2001; Brandt et al. 2005). On the one hand, polygynous colonies are probably better protected against social parasites due to their often larger colony size and they have a higher chance that one of the queens survives the attack (Foitzik and Herbers 2001). On the other hand, multiple-queening is thought to make colony odor more complex and therefore decreases the capability of discriminating between nestmates and alien ants, including social parasites (Breed and Bennett 1987). Experimental manipulations of social parasite pressure have indeed resulted in changes in host colony size and queen number, but it is has been difficult to separate the effects of the social parasite from other ecological influences (Fischer-Blass B and Foitzik S, unpubl.). Though intraspecific variation in queen number suggests that the way in which new colonies are founded is strongly influenced by ecological features, it is not yet clear whether all queens in facultatively polygynous species can choose between various alternative dispersal tactics or whether the latter are associated with genetic

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polymorphisms (and are thus correctly termed alternative strategies, Gross 1996). As shown above, independently founding queens may differ considerably in size or other morphological traits from queens, which found new colonies in a dependent way. In the red imported fire ant, Solenopsis invicta, the exchange of brood between nests of different queen number suggested that queen size and weight are strongly influenced by the social environment (Keller and Ross 1993), though other data indicate a strong genetic component (Keller and Ross 1998; Ross and Keller 1998). Similarly, crossbreeding experiments show that wing loss in queens is genetically determined in Leptothorax sp. A and Myrmecina graminicola (Heinze and Buschinger 1989; Buschinger 2005), and queen size in Temnothorax rugatulus (Rüppell et al. 2001b) and T. curvispinosus (Linksvayer 2006) and wing loss in an Australian species of Monomorium (Fersch et al. 2000) are also influenced by genotype.

6.3

Partitioning of Reproduction Among Female Sexuals

The presence of multiple reproductives per colony introduces a conflict about the partitioning of reproduction (reproductive skew), whose dynamics have been explored in a large number of “optimal skew” models (Reeve and Ratnieks 1993; Johnstone 2000). In general, reproductive skew can be affected by various factors, such as the relatedness between interacting individuals, their fighting strength, and ecological constraints on solitary nesting. Hence, environmental conditions, which favor multiple queening, may also lead to unequal partitioning of reproduction, i.e., “high skew”. In ants with multiple queen colonies, reproduction appears to be either completely monopolized by a single, socially dominant queen (“functional monogyny”, Buschinger 1968), or distributed among all queens according to their innate fertility without visible social hierarchies (e.g., Bourke 1991; Hannonen and Sundström 2002; Rüppell et al. 2002). In contrast to polistine wasps (e.g., Reeve et al. 2000), dominance relationships resulting in intermediate skew appear to be rare in ants. Dominance hierarchies, in which the top-ranking female monopolizes reproduction, are widespread in ants without morphologically distinct queens, in which one or a few mated workers take over reproduction (e.g., Monnin and Peeters 1998; Monnin and Ratnieks 2001; Cuvillier-Hot et al. 2002). In contrast, mated queens typically lay more or less equal numbers of eggs and also contribute similarly to the sexuals produced. Notable exceptions are functionally monogynous formicoxenine ants (Buschinger 1968). In Formicoxenus quebecensis, Leptothorax gredleri, and nearctic L. sp. A, queens engage in aggressive interactions after hibernation through which they establish dominance hierarchies, in which only the highest-ranking individual develops its ovaries (Heinze 2004). Several closely related species, such as Leptothorax muscorum and L. canadensis, are facultatively polygynous and in multiply queened colonies all queens lay eggs without evidence for dominance hierarchies. Optimal skew models have been used to investigate why queens fight in some species but are mutually tolerant in others. While queen–queen relatedness appears to be similar in polygynous and functionally monogynous species (Heinze 1995) and

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reproductive skew was also not significantly associated with relatedness in polygynous colonies of L. acervorum from England (Hammond et al. 2006), habitat preferences are strikingly different. Facultatively polygynous species live in uniform, coniferous forests, where nest sites are widely distributed over a large area and unlikely to be limited. In contrast, functionally monogynous species prefer habitats that are typically patchy: dry islands in spruce bogs, sunny patches at the edge of dense forests, etc. Bourke and Heinze (1994) suggested that colony founding is so difficult in such patchy habitats that young queens, who return into their maternal nests, can be forced to tolerate high skew. In contrast, young queens that are suppressed by the dominant in extended habitats have the chance to emigrate and found their own nests solitarily at least after hibernation. Of special interest is the case of L. acervorum, which is functionally monogynous at the edge of its distribution in light forest patches in Hokkaido, Alaskan forest-tundra and relatively warm and dry pine forests at Sra. de Alborracin in Spain (Ito 1990, 2005; Heinze and Ortius 1991; Felke and Buschinger 1999) but facultatively polygynous in most other studied populations throughout central and northern Europe (e.g., Buschinger 1968; Bourke 1991; Hammond et al. 2006). This species provides an interesting study system to investigate the flexibility of queens concerning the degree of reproductive skew. Queens from facultatively polygynous populations have been observed sporadically to engage in aggressive interactions, in particular when the ratio of workers to queens dropped to very low values. For example, queen antagonism occurred in two colonies of L. canadensis after most workers had died during hibernation and could be elicited in L. acervorum from a polygynous population at Merano, northern Italy, by experimentally removing 50% of the workers (unpublished results). This might suggest that the behavioral repertory of dominance interactions exists also in species or populations in which queens are typically tolerant of each other. Experiments in which colonies are transferred between patchy and uniform habitats or queen pupae are transferred between functionally monogynous and polygynous colonies are still missing. It would be interesting to know whether young queens from a population in which aggression is normally absent readily engage in dominance interactions when they are exposed to the typical social environment of a functionally monogynous colony.

6.4

Queen Mating Frequency

Multiple mating (polyandry) in social insects is a rather uncommon phenomenon and the causes for variation between species are as yet not completely understood. Large effective mate numbers are mostly restricted to taxa with very large colony sizes, such as honeybees and some vespine wasps and ants (Keller and Reeve 1994; Boomsma and Ratnieks 1996; Strassmann 2001; Crozier and Fjerdingstad 2001). Several arguments that are well known from the discussion about the evolution of sex have been used to explain the origin of multiple mating in social insects. For example, polyandry might be favored when parasite pressures are high or when ecological conditions vary (Schmid-Hempel and Crozier 1999; Brown and Schmid-Hempel 2003).

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The evolutionary transition from single to multiple mating in fungus-growing ants appears to be associated with the necessities for high genetic diversity in the more advanced genera, whose large colonies are fully dependent on fungus-gardens in large, subterraneous chambers (Villesen et al. 2002). The requirements for multiple mating apparently are lost during the evolution of a socially parasitic life style. Though closely related with polyandrous species, queens of the parasite Acromyrmex insinuator have reverted to single mating (Sumner et al. 2004). An association of multiple mating and colony size has been reported from vespine wasps (Foster and Ratnieks 2001) and Pogonomyrmex harvester ants, where queens mate singly in socially primitive species with comparatively small colonies but multiply in the more advanced Pogonomyrmex s.str., whose colonies may have thousands of workers (Gadau et al. 2003; Rheindt et al. 2004). Mating frequency often varies within species, but neither the causes nor the consequences of this variation are well understood. Colonies of Pogonomyrmex occidentalis with an increased mating frequency were shown to grow faster, probably because of a lower pathogen load or increased worker diversity (Wiernasz et al. 2004). Alternatively, associations between colony-level traits and mating frequency may arise from high-quality queens having more mates. Lasius niger queens that were heavier at the time of the mating flights were more likely to mate with multiple males and stored more sperm than lighter queens (Fjerdingstad and Keller 2004). When the effects of multiple mating and initial queen weight were considered simultaneously, any effects of mating frequency on colony performance vanished and colonies with singly and multiply mated queens were no longer different (Fjerdingstad et al. 2003; Fjerdingstad and Keller 2004). Mating frequency probably also varies with operational sex ratio and might thus be indirectly associated with ecological parameters, for example via population density (Boomsma and van der Have 1998). Assuming queens benefited from sampling the genetic diversity of males during their mating flights, they would mate less frequently when encountering only males from a few colonies. Multiple mating may play a role in maintaining genetic diversity in species where mating predominantly occurs in the maternal nest and involves siblings, but occasionally also adopted alien sexuals, as in Cardiocondyla (e.g., Schrempf et al. 2005; Lenoir et al. 2007). Furthermore, adverse environmental conditions have been suggested to be responsible for the low mating frequency of honeybee queens on a Friesian island (Neumann et al. 1999). It is likely that future research will reveal considerable spatial and temporal variation in queen mating frequencies.

6.5

Colony Size at Maturity

The size of a mature insect society is probably one of its most significant features, but at the same time the one where variation is least understood. It is well known that average colony size is of crucial importance for a suite of social and ecological traits (Bourke 1999), including task allocation, information transfer (Pacala et al. 1996;

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Andersen and McShea 2001; Thomas and Elgar 2003), foraging strategies (Beckers et al. 1989; Thomas and Framenau 2005), parasitization rate (Schmid-Hempel 1998) and the nature and success of mutual policing (Nakata and Tsuji 1996; Heinze 2004). Furthermore, colony size has obvious consequences for the ecology of a species. For example, Palmer (2004) showed that the outcome of interspecific competition in acacia ants parallels differences in their average colony size, with the species with the largest colonies being on top of the dominance hierarchy of competing species. The causes of the enormous variation in colony size between species are undoubtedly complex and any discussion remains premature until a full-fledged theory of life-history evolution for social insects has been developed. Nevertheless, a number of advances have been made to determine the role of specific environmental factors. For example, in a superorganismic analogy to Bergmann’s rule, Kaspari and Vargo (1995) suggested that the larger average size of colonies of boreal ants compared to tropical ants might serve as a buffer against harsh environmental conditions, in particular cold: larger colonies were supposed to be capable of storing more nutrients and therefore to survive the long winters in boreal habitats better (but see Kaspari 2005). An intraspecific analysis in Leptothorax acervorum failed to corroborate this hypothesis. While worker size increased considerably from 40.5 to 70°N (Heinze et al. 2003), variation in colony size did not show a similar trend and was presumed to be determined by other parameters. Intraspecific variation in colony size at maturity might in general be simpler to interpret, though here, too, the necessary large base is still lacking. The availability of food has been shown to control colony size in Crematogaster, which live on Macaranga plants and feed exclusively on food provided directly or indirectly, via Homoptera, by their host plants (Itino et al. 2001). However, most ants are generalists and at least in some wood-dwelling ants in temperate forests, food appears to be less limited than nest sites (Herbers 1993). Indeed, a strong correlation exists between preferred nest site and mature colony size (Hölldobler and Wilson 1990). This holds as well in comparisons between as within species in particular in ants living in preformed nest cavities (Fig. 6.2). The largest Leptothorax acervorum colonies, with close to one thousand workers, live in tree stumps in the Alps and driftwood on the shore of the White Sea, while colonies under small, sun-exposed pebbles in Alaska typically consist of only a few dozen workers (Heinze et al. 2003). Similarly, colony size is positively correlated with the size of the nest site in Leptothorax gredleri (Foitzik and Heinze 1999) and Temnothorax nylanderi (Foitzik and Heinze 1998). Surprisingly little is known about the consequences of colony size on the reproductive output of insect societies. Large colony size might be associated with complex colony-level functioning and individual workers might be more specialized and have lower per capita productivity (Michener 1964; Karsai and Wenzel 1998). In contrast, Jeanne and Nordheim (1996) found that per capita output increases at least in the wasp Polybia occidentalis. It would be interesting to know whether the shape of the correlation between colony size and productivity differs between populations of different average colony sizes and how strongly ecological conditions constrain size at maturity.

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Fig. 6.2 Typical nest of Leptothorax. These ants live in decaying wood, mostly in cavities made by wood-boring beetle larvae. The size of the nest site appears to limit colony size

6.6

Colony Composition

Insect societies are per definition characterized by a more or less complex division of labor, which not only encompasses that between reproductives and nonreproductives but often also involves numerous classes of workers that are specialized for certain tasks. The ratio between different classes of workers affects colony performance, in particular in species, in which worker specialization is associated with a pronounced polymorphism (Wilson 1980; Oster and Wilson 1978; Hölldobler and Wilson 1990). Caste ratios may differ between populations (Yang et al. 2004), and a number of investigations have studied how flexibly the percentage of foragers or the ratio of large to small workers in a colony reacts to changes in the environment. For example, foraging activity, and possibly also the percentage of foraging ants, in seed-harvesting ants depends on the nature and availability of resources and the encounter-rate with competitors (Brown and Gordon 2000; Gordon 2002; Sanders and Gordon 2003). Wilson’s (1983) “pseudomutant” studies on Atta leaf-cutter ants documented how the elasticity in the behavioral repertory of individual workers results in social homeostasis. When he experimentally removed most of the medium-sized workers specialized for leaf-cutting, the rate of this activity was unchanged because the remaining medium workers increased their activity and workers from other size classes engaged in this task. While in this study the production of the underrepresented size class from brood was not increased in response to the greater demand (Wilson 1983) and predation did not increase the percentage of soldiers in Pheidole dentata (Johnston and Wilson 1985), colonies of Ph. pallidula reacted adaptively

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to the presence of competitors by producing disproportionally more soldiers (Passera et al. 1996). Similarly, food supplementation altered caste allocation in Ph. flavens (McGlynn and Owen 2002). Several studies suggest that genetically different workers differ in their propensities to take over certain tasks. For example, in the colonies of honey bees, some genetic lineages specialize for undertaking, foraging for water, or nest guarding (Robinson and Page 1988, 1989; Page and Robinson 1990), and the variation in the initial behavior of freshly eclosed Temnothorax rudis workers was also interpreted as evidence for a genetic influence on division of labor (Stuart and Page 1991). Several recent studies have further documented that worker polymorphism in Camponotus and Acromyrmex, which is strongly associated with division of labor, has also a genetic basis (Fraser et al. 2000; Hughes et al. 2003; Julian and Fewell 2004). It remains to be clearly demonstrated that a higher genetic variability of the workforce increases colony performance. The respective data in honeybees are ambiguous (Fuchs and Schade 1994; Wojciechowski and Warakomska 1994; Arathi and Spivak 2001), and the benefits from genetic diversity are probably best explained in an increased disease resistance (Tarpy 2003; Seeley and Tarpy 2007).

6.7 Sex Allocation and Worker Reproduction How much insect societies invest in reproductives and in particular in male and female sexuals has found much attention since Trivers and Hare (1976) combined inclusive fitness theory and Fisher’s sex ratio theory. They predicted that workers in a monogynous, monandrous society favor a 3:1 investment sex ratio, paralleling the different relatedness of workers to female and male sexuals. Variation in relatedness asymmetries between colonies due to varying queen numbers and queen mating frequencies is supposed to influence reproductive decisions and to explain the phenomenon of split sex ratios (Boomsma and Grafen 1990, 1991). For example, colonies of the wood ant Formica exsecta with a single, singly mated queen reared predominantly female sexuals, while colonies with a multiply mated queen reared male sexuals (Sundström 1994). However, split sex ratios are also known from a number of species without relatedness asymmetries, and Meunier et al. (2006) showed that, averaged across species of social Hymenoptera, relatedness asymmetry variation explains merely 15% of sex allocation variation among colonies. Different resource availability (Nonacs 1986; Rosenheim et al. 1996) and resource quality (Bono and Herbers 2003) might contribute to this variation. Colonies with limited resources may benefit most from producing the cheaper sex, in the case of social Hymenoptera mostly males, while well-supplied colonies can afford to rear the more costly female sexuals. As predicted, food supplementation has indeed occasionally led to more female-biased sex ratios both in the field and the laboratory (Morales and Heithaus 1998; Deslippe and Savolainen 1995; Herbers and Banschbach 1998; Kikuchi et al. 2002; Bono and Herbers 2003; Brown and Keller 2005). However, the results were not always

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unambiguous, probably due to different ecological background (Backus and Herbers 1992; DeHeer et al. 2001; Herbers and Banschbach 1999). The availability of resources certainly varies with the abiotic and biotic environment, but may also be affected by social factors, such as colony size and the efficiency of workers. Trampus (2001) showed that genetic workforce diversity negatively affects cooperation in colonies of Temnothorax longispinosus. Though he did not directly investigate sex ratios, this phenomenon might proximately explain the widespread association between genetic heterogeneity and more male-biased sex ratios, not only in facultatively polygynous and polyandrous social Hymenoptera, but also in slave-makers and species, such as T. nylanderi, in which sex ratio varies with genetic structure without variation in relatedness asymmetries. As mentioned above, monogynous, monandrous colonies of Temnothorax nylanderi may fuse and young queens may usurp mature colonies when nest sites are limited. This results in mixed colonies, which produce a strongly male-biased sex ratio, though relatedness asymmetries remain unchanged as the workers are equally unrelated to the male or female sexual brood produced by the alien queen. Workers therefore do not benefit from manipulating sex ratios in a way they would in species with varying queen number or queen mating frequency (Foitzik and Heinze 2000). While from the field data alone it could not be excluded that a third factor simultaneously affects both sex allocation and the risk of being usurped or colony fusion, experiments, in which unrelated brood was added to laboratory experiments, clearly showed that lowered relatedness alone leads to male-bias (Foitzik et al. 2003). The suggested proximate explanation here might also lead to the correlation of sex allocation and average relatedness observed in facultatively polygynous Leptothorax acervorum (Heinze et al. 2001), where colonies with intermediate relatedness produced intermediate sex ratios. Detailed investigations in the interrelation between resource flow, genetic relatedness, and sex allocation are needed to clarify whether this proximate explanation can help to understand reproductive decisions more generally in social insects. Similar to sex allocation, reproductive allocation may be affected by ecological and genetic factors. One might expect that a high prevalence of pathogens and parasites, which decreases the life expectancy of a colony, changes the pattern of investment into colony growth and reproductives (Brandt et al. 2005). In the presence of some social parasites, Formica podzolica host colonies invested more heavily in rapid colony growth (Savolainen et al. 1996), while Temnothorax longispinosus colonies showed a higher investment in sexuals in areas with the slave-maker Protomognathus americanus (Foitzik and Herbers 2001). Where independent colony founding is difficult and young queens are forced to found their new nests by budding, the maternal colony should allocate more resources to workers than female sexuals. Indeed, queen-bias and queen morphology were found to be associated in Leptothorax sp. A. Colonies produced relatively large numbers of dispersing winged queens or smaller numbers of wingless queens (Heinze and Buschinger 1989). It remains unclear, however, whether the different investment in female sexuals is an adaptation to patchy environments or an epiphenomenon of the genetically determined queen polymorphism, but similar associations between

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reproductive and sex allocation on one side and founding tactics on the other have also been reported for other ants (Bourke and Franks 1995). Considering only the relatedness of workers to the male offspring that can be produced in a colony leads to the prediction that males favor worker-produced over queen-produced males in monogynous, monandrous societies, but queenproduced over worker-produced males in colonies with higher queen numbers or mating frequencies. That workers are most closely related to their own sons introduces reproductive conflicts between queen and workers and among workers, which finally result in queen policing or mutual worker policing (Ratnieks 1988). However, worker reproduction appears to be rare in social insects regardless of the genetic structure of the society, which calls for explanations other than kinship (Hammond and Keller 2004; Heinze 2004; but see Ratnieks et al. 2006; Wenseleers and Ratnieks 2006). As inclusive fitness is also affected by the costs and benefits of helping, workers probably are selected to refrain from egg laying when it is associated with costs, which decrease the reproductive output of the whole colony (Ratnieks 1988). Such costs can arise from inefficient division of labor, dominance interactions among workers, or inappropriate worker-brood ratios and may differ with ecological conditions. Experimentally increasing the worker-brood ratio by adding larvae in colonies of the clonal ant Platythyrea punctata indeed led to a reduction of brood survival (Hartmann et al. 2003), suggesting that natural colonies have a balanced worker-brood ratio that optimizes reproductive output. As yet, it appears that worker reproduction is absent from queenright colonies of most studied ant species (Hammond and Keller 2004; Heinze 2004). Among the six monogynous, monandrous ant species with worker reproduction listed by Wenseleers and Ratnieks (2006) in support of their hypothesis that the occurrence of worker reproduction varies with relatedness, are only two “normal” ants (Myrmica tahoensis and M. punctiventris), while all other species have a highly specialized life history: Protomognathus americanus and Polyergus rufescens are slave-making ants, in which workers generally have a higher reproductive potential (Heinze 1996), Dinoponera quadriceps is a queenless species with totipotent workers and dominance hierarchies, and Crematogaster smithi has a peculiar third female caste with a morphology intermediate between those of queens and workers, which is specialized for the production of viable, unfertilized eggs. Most of these eggs are eaten by the queen and the brood under unfavorable, dry conditions, but when the climate improves, some of these eggs might develop into males (Heinze et al. 1999).

6.8

Conclusions

Until two decades or so ago, many individual bird species were considered to be either monogamous or polygamous. Since then it has become evident from genetic analyses that social monogamy does not mean exclusive mating with

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only a single partner and that traditional views of avian mating systems are inadequate (e.g., Johnson and Burley 1997). The extra-pair copulation frequency of females differs tremendously both between and also within species in response to environmental factors, such as breeding density (e.g., Charmantier and Perret 2004). Similar paradigm shifts have occurred in social insects. For example, the belief that species are either monogynous or polygynous with the corresponding genetic colony structure has in part been replaced by the view that queen number is a highly plastic trait, which can show considerable intraspecific variation (e.g., Heinze et al. 1995; Ingram 2002; Pedersen and Boomsma 1999). Similarly, most other features of the complex phenotype of insect societies, be it sex allocation, caste ratios, and even sociality itself (e.g., Wcislo and Danforth 1997), react to ecological variation. It has to be admitted that many species are strictly monogynous or monandrous and others are always polygynous or polyandrous. Nevertheless, the determinants of intraspecific variation in the large number of species that are facultatively polygynous or polyandrous certainly deserve more attention. How much of this social plasticity is genetically determined and whether it is adaptive or results from ecological or historical constrains remains to be studied. Of particular interest is the possible occurrence of “cultural evolution,” i.e., the non-genetic transmission of certain features of the social phenotype from generation to generation. As mentioned above, the weight of female sexuals appears to be influenced by the social environment of the colony in the fire ant Solenopsis invicta (Keller and Ross 1993), and imprinting of young social parasites on the odor of the hosts present in their nests might explain host choice (Schumann and Buschinger 1994, 1995) and could establish similar “traditions.” It is a small step from acknowledging the importance of ecology for present-day insect societies to wondering about the role of ecology in the beginning of eusociality. This is well appreciated by social insect specialists who are familiar with the fact that Hamilton’s equation includes two terms – the costs and benefits of helping – that are strongly affected by ecological variation. However, researchers from outside this field often feel that social Hymenoptera are special because of their haplodiploidy and the resulting particular relatedness relationships. Nevertheless, ecological factors that have been and are significant in the establishment and maintenance of group-living in other animals are certainly of importance also in ant, bees, and wasps. Furthermore, once insect societies have evolved group-level novelties, such as division of labor, thermoregulation or air condition, natural selection at the level of the colony may override kin considerations and make the social structure relatively insensitive against variations in individual relatedness. Acknowledgements This work was supported by Deutsche Forschungsgemeinschaft (He 1623/17). This paper benefited from discussions with colleagues at the symposium “Social plasticity” at the IXth Congress of the European Society for Evolutionary Biology in Leeds, 2003, and the international symposium “Life cycles in social insects” in St. Petersburg, 2003. J.J. Boomsma and J. Liebig made helpful comments on the manuscript.

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Chapter 7

The Ecology of Social Evolution in Termites Judith Korb

Abstract Termites (Isoptera) belong to the classical eusocial insects and their resemblance to ant colonies is so striking that they are commonly known as ‘white ants’. However, the termites evolved social life independently, long before the ants. Their different ancestry also is reflected in several fundamental differences in the organization of the colonies. This chapter aims at summarizing the state-of-the-art in termite research and comparing the results with other social invertebrate and vertebrate systems in an attempt to reveal common principles underlying social evolution. First, I provide an overview of termites’ biology and classification. I continue with a summary on the ‘hunt’ for a genetical explanation of the evolution of termite’ eusociality. Using a case study, I summarize ecological factors favoring cooperation in a lower termite and show the relevance of these results for other termite species. Based on these results I outline the potential evolutionary transitions in termite eusociality. Finally, I compare the driving forces in termites with those in cooperatively breeding vertebrates and offer a potential explanation why eusociality rarely evolved in vertebrates, despite often strikingly similar ecological pressures in both groups.

7.1

Introduction: An Overview of Termite Classification and Biology

Termites (Isoptera) are the oldest social insects with a social life that dates back to the Cretaceous when they had dinosaurs as their contemporaries. In the oldest fossils from the Cretaceous (130 Mio), it is clear they were already social with characters strikingly similar to modern basal species (Thorne et al. 2000). Although

Judith Korb Department Biology I, University of Regensburg, 93040 Regensburg, Germany [email protected]

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their morphology was primitive, the Cretaceous termites were already reasonably diversified suggesting an origin in the upper Jurassic. Non-social termites, either fossil or recent, are unknown but termites, cockroaches (Blattaria) and mantids (Mantodea) form a natural assemblage (Walker 1922) and are commonly grouped as suborders of the Dictyoptera (Kristensen 1991). The relationship among the three lineages is controversial (Nalepa and Bandi 2000; Eggleton 2001). Some authors contend that the primary dichotomy lies between the Isoptera and (Blattaria + Mantodea), and others that Mantodea diverged first, with Blattaria and Isoptera either as sister groups, or with Isoptera nested within the Blattaria (Hennig 1981; Thorne and Carpenter 1992; Grandcolas 1994; Klass 1995; Kambhampati 1995). The weight of evidence now suggests the latter (Inward et al. 2007). Most likely, they form the sister group of the Cryptocercidae (woodroaches) (Eggleton 2001; Inward et al. 2007a). It is generally accepted that eusocial termites evolved from a subsocial ancestor (Thorne 1997; Shellman-Reeve 1997). Fossil and molecular data both suggest that eusocial termites evolved relatively rapidly from their non-eusocial ancestors, and with no intermediates in the fossil record, it difficult to resolve the phylogenetic relationships (Nalepa and Bandi 2000). The termites form a diverse group with over 2600 described species that range across 281 genera and seven families: Mastotermitidae (only 1 species: Mastotermes darwiniensis), Hodotermitidae, Termopsidae, Kalotermitidae, Rhinotermitidae, Serritermitidae, and Termitidae (Kambhampati and Eggleton 2000; Eggleton 2001; Inward et al. 2007b). Classically, they are grouped into the lower termites (all families except the Termitidae) and the higher termites (Termitidae), the latter constituting about 75% of all termite species (Kambhampati and Eggleton 2000). The phylogenetic relationship among the families is not completely resolved (Eggleton 2001; Lo et al. 2004) but Mastotermitidae is now generally accepted to be the most basal termite group (Fig. 7.1). Termopsidae, Hodotermitidae and Kalotermitidae are all basal to (Termitidae + Serritermitidae + Rhinotermitidae), although their relative positions within that part of the tree are disputed (Eggleton 2001). Most recent studies support a sister group relationship for Serritermitidae and (Termitidae + Rhinotermitidae). Recent molecular studies indicate that there is need for a major revision of the Rhinotermitidae that seem to be paraphyletic with the Termitidae nesting within this family (Lo et al. 2004). Based on their ecology, and particularly their nesting and feeding habits, termites can be grouped into two life types (Abe 1987, 1990): (i) One-piece type termites (Termopsidae, Kalotermitidae and Prorhinotermes within the Rhinotermitidae; hereafter called OP termites): These species live in their food and spend their entire colony life in a single piece of wood that serves as both food source and shelter. As these termites do not forage for new resources, the availability of wood in the nest is of prime importance for the maximum longevity and the stability of the colony. (ii) Multiplepieces type termites (including Abe’s intermediate type; hereafter called MP termites) (Mastotermitidae, most Rhinotermitidae, Serritermitidae, Termitidae): These species live in a well-defined nest that is more or less separated from the foraging grounds. The fact that workers can explore new food sources outside the nest typically means that the nest’s longevity is less limited by food availability than in the OP species

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(Fig. 7.1). This ecological classification is also reflected in the social organization of the colonies. Wood-dwelling OP termites have a flexible development in which workers are totipotent to explore all caste options (Lüscher 1974; Roisin 2000). In order to reflect this distinction, they have also been called false workers, pseudergates or helpers (Thorne 1996; Roisin 2000). However, the utility of these extra terms is unclear, the term pseudergate is confusing and should be avoided. Pseudergate was originally defined for individuals that develop regressively from nymphs (in termite terminology: instars with wing buds) into workers (Grassé and Noirot 1947; Noirot and Pasteels 1987). In practice, it is difficult to separate pseudergates sensu stricto from younger individuals as the former can regain the morphological appearance of the latter. These pseudergates sensu stricto are also not the only ‘workers’ in the nest, but the work force also consists of late instar larvae (in termite terminology: instars without wing buds) and nymphs (Noirot and Pasteels 1987; Thorne 1997). In contrast to the OP termites, all species of the MP type have a true, morphologically differentiated worker caste with reduced reproductive potential. This reaches its extreme in the higher termites where workers are terminally differentiated and cannot proceed to the alate stage (Noirot 1990). In these species, a bifurcation into the neuter (workers and soldiers) versus the sexual line exists that is set at an early instar (Roisin 2000). In some species of the Termitidae, caste fate appears to already be determined in the egg (Roisin 2000). Several other life-history traits correlate with this classification by nesting habit (see also Shellman-Reeve 1997). OP termites with their non-replenishable food source, have generally rather short-lived colonies (4–15 years in most species; Abe

Mastotermitidae (MP)

Hodotermitidae (MP)

Termopsidae (OP)

?

Kalotermitidae (OP) Serritermitidae (MP)

Rhinotermitidae (OP + MP) + Termitidae (MP) Fig. 7.1 Family-level phylogeny for termites after Eggleton (2001) and Lo et al. (2004). The relative position of the three grey families is not clearly resolved. OP Wood-dwelling, one-piece nester termites, in which food and nest are identical; MP Multiple-pieces nester termites, in which nest and food are separated (for more information see text)

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1987; Lenz 1994) of small sizes (600–8,000; Lenz 1994). In contrast, MP termites are relatively long-lived (up to several decades; Roonwal 1970; Grassé 1984; Shellman-Reeve 1997; but see Soki et al. 1996 for short life-span of some Termitidae) and can reach large colony sizes (up to 1–5 million; Nutting 1969; Darlington 1979; Darlington et al. 1992; Lenz 1994). There, the life-span of a colony seems to be chiefly limited by predation (Bodot 1961; Longhurst and Howse 1979; Longhurst et al. 1979; Levieux 1983; Abe and Darlington 1985; Darlington 1986; Gotwald 1995; Korb 1997; Korb and Linsenmair 1999, 2001; Noirot and Darlington 2000) and sometimes competition (Leponce et al. 1997; Lepage and Darlington 2000; Korb and Linsenmair 2001), while the availability of nesting space and the fecundity of the reproductives sets the maximum colony size (Grassé 1984; Lenz 1994). There is a high degree of task specialization within colonies, reaching its peak in the Termitidae in which four morphological castes can often be distinguished that additionally exhibit age polyethism (Gerber et al. 1988; Veeranna and Basalingappa 1990; Lys and Leuthold 1991; Traniello and Leuthold 2000). The division into OP and MP termites is not identical with the classical division in lower and higher termites (Fig. 7.1). The higher termites are confined to the family Termitidae, which are MP termites, but there are also other MP termites (i.e., Mastotermitidae, Hodotermitidae, Serritermitidae and the Rhinotermitidae with the exception of Prorhinotermes) that belong to the lower termites. On the other hand, however, all OP termites are lower termites.

7.2

Evolution of Sociality in Termites: the Hunt for a Genetic Explanation

The correspondence between life type (log and nest) and social organization in the termites highlights the central importance of ecological parameters in their evolution (Higashi et al. 1991, 2000). Yet, like in other social insects, explanations for the evolution of termites’ sociality has mainly focused upon genetics and specifically kinship relatedness, which has become relatively easy to quantify with the advances in genetic techniques in the last 20 years. The altruistic behavior seen in insect workers, in which they reduce their lifetime reproductive success (direct fitness) in order to increase the fitness of the reproductives, can be explained by kin-selection theory: the propagation of genes via closely relatives (Hamilton 1964; Maynard Smith 1964). According to Hamilton’s rule, altruism will be favored when rb > c, where r is relatedness between the recipient and actor and b and c are the benefit and cost of the action to the actor and recipient respectively (Hamilton 1964). The unusually high relatedness between sisters in the social Hymenoptera that occurs due to their haplodiploid genetics (males derive from haploid unfertilized eggs and females from fertilized diploid eggs) was initially thought to explain the multiple origins of eusociality in this insect order and the female preponderance in these colonies (Hamilton 1964, 1972; for a recent discussion: Bourke and Franks 1995; Crozier and Pamilo 1996; Queller and Strassmanm 1998; see Chap. 1 and

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Chap. 6). In the diploid termites, no such easy genetic explanation was at hand to explain their resemblance to ant colonies, which is so striking that they are commonly known as ‘white ants’. The discovery of chromosomal translocations, in which a tight linkage of genes to the sex chromosomes occurs, seemed to provide a welcomed haplodiploidy analogy (Luykx and Syren 1979; Lacy 1980). However, chromosomal translocations are not common in the clades thought to be closest to the non-eusocial ancestor of termites and the species in which translocation occurs do not show the predicted sex-discriminative behavior (Crozier and Luykx 1985; Hahn and Stuart 1987; Leinaas 1983; Vinque and Tilquin 1978; Roisin 2001). Another candidate genetic explanation was that of inbreeding-outbreeding cycles (Bartz 1979). Bartz suggested that unrelated alates found new colonies but are later replaced as king and queen by their offspring, which remain in the colony and breed together. After several cycles of such replacement, highly inbred and therefore highly homozygous, alate offspring are produced. Assuming that such inbred alates mate with unrelated, but also inbred partners, relatedness asymmetries comparable to those of the Hymenoptera could arise: offspring from the colony founders are more related to each other than they would be to their own offspring and raising full siblings could become selectively favored. However, although inbreeding does frequently occur in termites, neither are the alates only produced by inbred reproductive nor is the number of inbreeding cycles high enough to produce highly inbred offspring (Myles and Nutting 1988; Atkinson and Adams 1997; Thompson and Herbert 1998; Husseneder et al. 1999; Shellman-Reeve 2001). Thus, the hunt for a special genetic explanation for the evolution of eusociality in termites faltered and seemed to ultimately fail. A similar situation emerged in the eusocial Hymenoptera where the perceived importance of the haplodiploidy hypothesis faded as it became clear that haplodiploidy will only promote altruism relative to diploidy under rather restricted conditions, and eusociality was discovered in more and more non-haplodiploid species (Queller and Strassmann 1998). The costs and benefits terms in Hamilton’s rule have at last gained the equal footing that they deserve alongside relatedness in explanations of altruism. As a result, explanations for why eusociality has evolved so often in certain insect groups have taken on a distinctly ecological flavor. However, studies that quantitatively tested any factors either ecological or genetic are scarce in the termites. In the next section I will present a case study that tried to fill this gap.

7.3 7.3.1

A Case Study: Cryptotermes secundus Workers

The Australian drywood termite Cryptotermes secundus (Kalotermitidae) occurs in dead mangrove trees that have a patchy distribution (Miller and Paton 1983; Korb and Lenz 2004). As is typical for OP termites, the workers are totipotent and able

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to develop into all possible castes (Fig. 7.2): (i) sterile soldiers, (ii) replacement reproductives via one neotenic molt when the same sex reproductive of the colony dies, or (iii) winged reproductives, which leave the nest to found a new colony, via several nymphal instars (Korb and Katrantzis 2004). In contrast to eusocial Hymenoptera or MP termites with morphological castes, therefore, being a worker is not a lifetime strategy but rather a developmental tactic that can be abandoned if conditions change. The basis for this developmental flexibility are progressive (increasing body size and/or wing buds), stationary (no morphological change), and regressive (decreasing body size and/or wing buds) molts (Korb and Katrantzis 2004). Regressive molts are a particularly unusual and important feature of their development because it allows individuals that have already started to develop towards sexuals to partially regress their development and become again a worker (pseudergates sensu Grassé and Noirot 1947) lacking any signs of wing buds. Collections of natural field colonies together with laboratory and field experiments have revealed that caste development in C. secundus workers is influenced by internal (e.g., colony size) as well as external factors (Korb and Lenz 2004; Korb and Schmidinger 2004; Korb and Katrantzis 2004; Korb and Fuchs 2006). The development into winged sexuals is largely regulated by season (Korb and Katrantzis 2004). Over a 7-month period, individuals gradually progress through five successive nymphal instars to become alates by August when the annual nuptial flight takes place. During this developmental period there appear to be deadlines for each successive nymphal instar on the way to becoming a winged

Egg

Larvae

‘Worker’ + Neotenic Reproductive

‘Worker’

Nymph

Primary Reproductive

Soldier (sterile)

Fig. 7.2 Simplified developmental pathway of Cryptotermes secundus (Kalotermitidae). Eggs develop via larvae into workers. Then workers can develop (i) progressively via nymphal instars into winged sexuals (alates) that leave the nest to found a new colony as primary reproductives, (ii) into sterile soldiers, or (iii) via one neotenic molt into a replacement reproductive. The development from nymphs to workers is reversible via regressive molts. Photos: J. Korb

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reproductive. Those individuals that do not reach a certain instar by a certain date (week) will regress their development and molt back into workers without wing buds (pseudergates sensu Grassé and Noirot 1947). Deadlines for earlier instar nymphs occur sooner than for older instars, which may be indicative of a reduced investment in progressive molts in response to the reduced likelihood of making the final deadline. These deadlines probably function to ensure that only individuals that are competent and well nourished to successfully disperse, fully develop into alates. This developmental strategy is in line with a mechanism suggested by Roisin (1994) for the evolution of workers in termites: According to the loser hypothesis, the termite worker caste evolved from individuals incapable of developing into sexuals. However, the ‘loser’ phenotype in C. secundus was not associated with aggressive manipulation by siblings or parents (Korb 2005) as suggested by Zimmerman (1983) and Myles (1986). Being a worker rather seems to be a conditional strategy (sensu Gross 1996) where individuals less competent for founding their own nest stay in the natal colony. Data for C. secundus show that this development can be reversed again and that regressed workers can later resume alate development (Korb, unpubl. data). In addition to this seasonal regulation, alate development is also influenced by food availability in the nest (i.e., size of the wood the colony is nesting in) that adjusts the number of remaining workers versus dispersing sexuals (Korb and Katrantzis 2004). When the wood size reaches a certain threshold (< c.a. 2.5 cm3 per termite), individuals begin progressive nymphal development earlier in the year. Placing colonies 2 months after the nuptial flight into wood blocks below the threshold size immediately elicits progressive development, meaning that the first nymphal instars occur 3 months earlier than under abundant food conditions. As a result, more individuals reach the molt deadlines and mature into winged sexuals than in colonies with abundant food (Korb and Katrantzis 2004). Despite the precocious start to progressive development, the sexuals in these food limited colonies still leave the colony at the annual nuptial flight because their development slows down as they reach late instar nymphs (Korb and Katrantzis 2004). This increase in dispersal as sexuals makes adaptive sense for log dwelling termites like C. secundus because as the log diminishes, so too does the probability they will be able to reproduce in the natal colony before the wood runs out (see below). A central component of this response is the termites’ impressive ability to detect changes in the size of their log and so predict colony longevity (Korb and Katrantzis 2004). In C. secundus the loss of wood from the log occurs gradually by the termites own consumption of the wood but also suddenly when cyclones or heavy thunderstorms fragment their trees (Korb and Lenz 2004). Correspondingly, the termites cannot rely on extended excavations to measure wood availability. Instead, the termites continually sense the amount of wood from the vibrations generated during wood gnawing (Lenz 1994; Evans et al. 2005). These vibrations constitute reliable and fast cues of food availability. This predictable variation in food availability/colony longevity probably selects for the flexible development of workers in OP termites (Korb and Katrantzis 2004). This situation contrasts with the MP termites that leave their nest to exploit resources. They reduce the long-term

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food variability but experience short-term variation in food supply that lacks predictable cues allowing a plastic developmental response. The obvious importance of ecology in the reproductive development of C. secundus contrasts sharply with variation in relatedness, which appears to have little effect. Colonies are founded monogamously (mainly by outbred pairs) resulting in a withincolony relatedness of r = 0.5. However, variation in between- and within-colony relatedness is common due to two key processes, (a) reproductive replacement: the primary reproductives die and are replaced by inbred neotenic reproductives (increase in relatedness; c.a. 16% of colonies) and (b) colony fusion: colonies that were independently founded in the same tree meet and mix during colony expansion (decrease in relatedness; > c.a. 25% of colonies) (Korb and Schneider 2007). Fusion creates a single colony containing related and unrelated nestmates, and often, both reproductives of one of the original colonies are killed during fusion, which means that the workers of this colony are unrelated to the offspring produced after colony fusion. The decrease in relatedness resulting from fusion might be expected to cause more workers to leave the colony as dispersing sexuals. This is because the reduced relatedness means that the inclusive fitness benefits that they can get from helping other members of the colony will also reduce. However, there is no evidence that this occurs (Korb and Schneider 2007). This is not because the termites cannot detect the fusion event: workers can be observed do change certain behaviors (Korb and Schneider 2007) and seem to have the ability to even recognize kin (Korb 2006; Fuchs and Korb, unpubl. data). Also the developmental response of workers in inbred colonies does not seem to be linked to their increased relatedness, but to a higher likelihood of inheriting the natal colony (Korb and Schneider 2007). The discovery that the workers stay in the colony even when they are not related to the king and queen can be explained by data that suggest they are not workers at all (Korb 2007). If the workers stay in the colony in order to help rear the colony’s offspring, then increasing the number of offspring should increase the benefits of working and decrease the likelihood that a worker develops into a dispersing sexual. However, an experiment that added young instars to nests showed the number of offspring to raise did not affect the number of worker individuals developing into dispersing sexuals. Furthermore, the additional young instars nevertheless survived, although worker individuals left the colony (Korb 2007). Detailed behavioral observations further confirmed that the workers were not helping to rear offspring (Korb 2007). There is no brood care, and foraging, an important and risky task normally carried out by workers of social insects, is unnecessary as the colony lives within its food. Interactions between individuals in general are rare and proctodeal trophallaxis (= anal feeding) and allogrooming are not altruistic because each individual receives as much as it provides. So why do workers remain in the colony if they gain no indirect benefit from raising siblings? It appears that they are hopeful reproductives. A model based upon long-term field data revealed that the number of individuals staying at the nest can be explained by the probability of inheriting the nest versus founding a new colony (Korb and Pirow, in prep). The probability of founding and inheritance are both very low (< 1%) and certainly within the same order of magnitude (Korb and Schneider

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2007). The exact values depend on the colony size, the age of the reproductives, and the potential longevity of the nest and these three variables can be used to accurately predict the number of individuals developing into dispersing sexuals in field colonies (for similar results in a stenogastrine wasp see Chap. 4). In summary then, it appears that C. secundus workers should be regarded as hopeful reproductives rather than true altruistic workers that stay for kin’s sake. This explains why ecological factors like food availability, i.e., the potential longevity of the nest which determines the value of inheriting it, influences the development of individuals, whereas variation in relatedness among colony members has no effect.

7.3.2

Soldiers

In contrast to the workers, C. secundus soldiers that make up less than 5% of all colony members, are a true altruist caste that gains indirect fitness benefits (Roux and Korb 2004). They are sterile and represent a developmental endpoint as they lost their capability to molt. They are morphologically highly specialized with large mandibles and a plug-shaped head that is heavily sclerotized and used to effectively block the wooden nest galleries (Fig. 7.3). An experiment in which soldier development was inhibited has shown that soldiers increase the reproductive success of their colony and therefore gain indirect fitness benefits (Roux and Korb 2004). However, in contrast to general assumption, their function does not seem to lie in the defense of the colony against predators. Predators are extremely rare in C. secundus because the wooden nest structure is a very effective protection preventing predators from entering the nest. Indeed, over 5 years of fieldwork involving more than 600 studied colonies no predators or traces of predation were found (Korb and Roux, in prep.). The main threat for C. secundus colonies seems to be competitors

Fig. 7.3 Phragmotic head of a Cryptotermes secundus soldier. Photo: Birgit Lautenschläger

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that live in the same tree and consume the non-replenishable wood. Beetle larvae (especially Buprestidae) are very common (in c.a. 25% of all trees) that consume considerable quantities of wood and render contacted wood unpalatable to termites. However, these are not repelled by the soldiers (Korb and Roux, in prep.). Beetle larvae are attacked by workers as well as soldiers but with little effect. Often the beetle larva is sealed off and continues to consume the wood from its sealed cavity. The main colony benefit provided by soldiers seems to occur through attacks on other termites, either of the same species or of the congeneric species C. domesticus that has very similar habitat requirements like C. secundus. As mentioned earlier, intraspecific encounters are quite common and arise when colonies founded in the same tree meet. When this occurs, the number of soldiers per worker present in a colony is a key factor that determines the survival success of a colony’s reproductives (Korb and Roux, in prep.). Thus, intraspecific competition (and probably also congeneric competition with C. domesticus) seems to be the prime factor selecting for the maintenance of soldiers in C. secundus. That there is selection on the occurrence of soldiers, despite a lack of predation, is supported by a morphometrical study (Roux et al., in prep.). The dimensions of the plug-shaped soldier heads vary among colonies, but this variation correlates with the variation in gallery dimensions. Colonies with soldiers that have larger head widths inhabit nests with larger gallery dimensions, while this does not hold, for example, for soldier body size. This correlation is also not just a consequence of soldiers being the constructors of the galleries because they are excavated by the workers. Furthermore, the variability in the dimensions of defensive traits of soldiers’ morphology is consistently lower than those of non-defensive traits. This together with negative allometric slopes of defensive traits suggests that the defensive morphology of soldiers is indeed under stabilizing selection.

7.4

7.4.1

Relevance of the Case Study: Comparison with Other Termites Workers

Many of the features of C. secundus sociobiology are likely to apply to other log termites that live in a confined piece of wood (about 17% of all termite species; Kambhampati and Eggleton 2000) because, like C. secundus, they all have the following traits: (a) Flexible development: workers seem to be able to explore all caste options (see above) (Shellman-Reeve 1997; Roisin 2000; Thorne and Traniello 2003) and all these species are characterized by a high potential of workers to develop into neotenic replacement reproductives (Myles 1999), thus having the chance to inherit the natal breeding position.

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(b) Well-protected nest: individuals are well sealed off against predators and extremes of climatic variation. Thus, survival rates in the nest are high. (c) No foraging trips: living inside their food again improves survival and also reduces the value of care for other nestmates as all individuals have easy access to food. (d) Predictable resources: the quality of the nest can be quickly and reliably measured. Vibrations generated by wood gnawing are the cues used to assess food availability (Lenz 1994; Evans et al. 2005). Thus, individuals have the information necessary to adaptively adjust their development to potential reproductive opportunities. (e) Predictable change in resource availability: the quality, and thus the breeding opportunities, in the natal nest changes predictably. All colonies inevitably experience a shortage of the non-replenishable food source and thus the disappearance of their nest. This together with the reliability of the cues to measure nest size seems to select for a high developmental plasticity, because both reliable cues and predictability are parameters selecting for plastic development (Nijhout 2003). This may explain the correlation between the wood-dwelling life type in OP termites and their flexible caste development (Korb and Katrantzis 2004). These shared features suggest that the workers of all wood-dwelling termites are in a similar situation to those in C. secundus that do not seem to be true workers at all. In support of this, reports exist for many species that colonies with low food availability produce more alates than colonies with high resources (Buchli 1958; La Fage and Nutting 1978; Lenz 1976, 1994; Korb and Lenz 2004).

7.4.2

Soldiers

The results from C. secundus also seem to apply more widely to the soldiers in other termites. Intraspecific competition seems to form a major threat to many lower termites with evidence from genetic studies that colony fusion is common in several species (Clement 1986; Bulmer et al. 2001; Goodisman and Crozier 2002; DeHeer and Vargo 2004). This suggests that colonies do not necessarily consist of closely related nestmates, as has generally been assumed and that competition both within and between termite species is very important. Support for the role of intraspecific competition in the occurrence of soldiers was recently provided by Thorne et al. (2003), who found that reproductive soldiers in Zootermopsis nevadensis are more common in colonies with a fusion history. These reproductive soldiers are a peculiarity of the family Termopsidae and are unlikely to be representative for termite soldiers in general (Roisin 2000). They are not individuals with a reduced reproductive capacity such as the sterile soldiers of other termites. Rather they are neotenic reproductives with soldier-like traits and should therefore

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better be called soldier-like neotenics/reproductives (Thorne 1997; Roisin 2000). Nevertheless, the Zootermopsis study shows the importance of intraspecific encounters as a selective force for the development of defensive traits; in this case of reproductives which after a fusion event seem to have a higher chance to inherit the colony as replacement reproductive (Thorne et al. 2003). This links back to the occurrence of workers in C. secundus: in both cases, in C. secundus and Z. nevadensis, inheritance opportunities, and thus direct breeding benefits in the nest, seem to be the driving forces for their occurrence (Myles 1988). Indeed, such selection for the soldier caste was probably also important ancestrally because conspecific competition is likely to predate the major termite predators of extant termites (ants and mammals).

7.5

Outline for the Evolutionary Transitions in Termites Eusociality

The view that OP termites with their flexible development reflect the ancestral state in termite evolution has been challenged (Thompson et al. 2000) but the molecular data currently still fail to resolve the relevant phylogenetic relationships (Fig. 7.1; Grandcolas and D’Haese 2002; Thompson et al. 2004; Inward et al. 2007b). Yet, other results leave less doubt about the basal position of the wood-dwelling life type (Parmentier and Roisin 2003; Parmentier 2006; Korb, in press). Therefore, I use it here to develop a tentative outline for the evolutionary transitions of eusociality in the termites (Fig. 7.4). The hemimetabolous subsocial termite ancestor, like the woodroach Cryptocercus punctulatus, most likely lived inside wood that served as nest and food (e.g., Nalepa 1994; Thorne 1997; Fig. 7.4 Ancestor). Such a nesting type provided (a) a longlasting stabile, but non-replenishable food source, (b) a safe nest that is largely protected against predators and hostile environmental conditions, and (c) low-quality food that results in slow development and which can only be exploited with the help of symbionts. Thus the nest represented a safe haven compared to the hostile and uncertain environment encountered during dispersal. Such conditions select for alternative reproductive tactics, namely staying in the nest to inherit the colony, as is also found in many aphids and thrips (see Chaps. 2, 3, 12; Stern and Foster 1997). These conditions also favor a flexible development (Fig. 7.4, stage I: Evolution of staying immatures): Firstly, it is important to be able to replace the reproductives immediately after their death (evolution of neoteny) and, secondly, to react to changing nest conditions that will inevitably occur when the food is exploited or when environmental hazards like thunderstorms suddenly destroy the nest (evolution of different molting types). Functional reproductives should not be killed as they are the parents of staying individuals; so kin selection is a very important component in this system as it reduces conflicts and guarantees group stability. Thirdly, as group size increases the chances to inherit decrease and competition among siblings for the breeding position increases. This should select for some

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Pre-adaptations: ‘Save haven’ nesting site hemimetabolous, flexible development abundant, low-quality food slow, flexible development High mortality risk during dispersal of the alates

Stage I: Staying immatures

Selection on: more flexible, conditional development Increased probability to inherit the natal nest as offspring are still in the nest when parents die Selection on: flexible development and neoteny aggregation of individuals emergent property advantages of group living

Stage II: Soldiers

Increasing competition among colonies Selection on: improved defense sclerotization (terminal instar) reduced longevity Selection on: evolution of a soldier caste increasing synergistic benefits of group living

Stage III: True workers

increasing colony size Food becomes a limiting resource Selection on: exploitation of new food sources transition to ‘MP’ termites increasing colony sizes division of labor, workers with reduced reproductive potential, but indirect fitness gains

Fig. 7.4 Scenario for the evolution of termite eusociality. For further information see text

individuals leaving the nest even if it is still long-lasting. Those leaving individuals should be the most competent to do so (for a detailed discussion see Korb and Schmidinger 2004). The competence of different individuals may be ‘tested’ by developmental deadlines; individuals failing to reach them in time have to develop back to be ‘tested’ again for the next nuptial flight (see above). Thus, this evolutionary

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stage (Fig. 7.4, stage I) would largely correspond to the ‘worker’ stage in C. secundus. Note that at this stage there is no help in raising siblings because this is unnecessary; as hemimetabolic insects, the young larvae are quite independent and food is easily accessible to everybody. The result of this evolutionary step would be family groups, with group sizes depending on wood size and inheritance opportunities. At this stage, living in a group may offer additional advantages such as improved thermoregulation, parasite resistance, or construction capacities (Rosengaus et al. 1998; Rosengaus and Traniello 2001; Traniello et al. 2002; Korb 2003; Korb and Heinze 2004). Also division of labor may evolve. All these advantages may offer further incentives for staying at the nest. On the other hand, intraspecific competition with colonies that had been founded in the same tree will increase as the groups are long-lived, and the likelihood increases that they will meet because of nest expansion. This would strongly select for a defensive morph, which may have a reproductive potential, like the soldier-like neotenics in the Termopsidae (Thorne et al. 2003), or which may not, like soldiers in all other termites and in the aphids and thrips (see Chaps. 2 and 3) (Fig. 7.4, stage II: Evolution of soldiers). As there is strong selection for a defensive morph to be sclerotized, these individuals lose the capability to molt. Therefore the defensive morph presents a terminal stage, again either a fertile soldier-like neotenic or a sterile soldier. Why soldier-like reproductives are limited to the Termopsidae and soldiers of all other termites are sterile remains an open question. Defenders, however, make up only a low proportion of the group as the main protection against predators is provided by the nest (Noirot and Darlington 2000). In the case of soldiers, these groups can now be considered eusocial insect colonies similar to those represented by the recent wood-dwelling termites in which soldiers make up < 5% of all colony members (Haverty 1977; Henderson 1998). Due to their small numbers, the indirect fitness gains of sterile soldiers are high (Roux and Korb 2004), compensating for the high costs of the defensive task. At this evolutionary stage (Fig. 7.4, stage II), the limiting factor for the colonies becomes the restricted amount of food, set by the nest size, and resulting in increasing intraspecific competition. This constitutes a strong selection pressure to exploit new food sources, also offering the possibility to choose higher-quality food that allows faster development (e.g., selection of partly decayed wood that is easier to digest and where the inhabiting microorganisms present an additional nitrogensource). However, along with the exploitation of new food sources comes the cost of increased predation pressure during foraging. This has the consequence that getting food is no longer cost-free and not easily accessible for all termites, especially for the young instars and the reproductives. Now brood care becomes obligatory and it is associated with increased mortality costs during foraging. These costs are compensated by the indirect fitness gains of raising siblings (Fig. 7.4, stage III: Evolution of true worker). Whether the step to sibling brood care only evolved at this late stage or whether some OP termites already show brood care, because it enhances development, needs to be investigated. With the exploitation of new, better-quality resources colony size could increase, leading to an effective division of labor with several castes specializing on different colony tasks. The highest sophistication in recent

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termites occurs in the Termitidae, and especially in the fungus-growing termites (Macrotermitinae), where up to four different sterile castes exist in addition to temporal polyethism within castes (Traniello and Leuthold 2000). The Termitidae represent those termites that are evolutionary and ecologically the most successful, constituting about 75% of all recent species (Eggleton 2000) and being the most important decomposers in many tropical ecosystems (Deshmukh 1989; Bignell and Eggleton 2000). In summary, current studies suggest that, in contrast to previous assumptions, the first critical step to eusociality in termites was probably not offspring staying at home to raise siblings but rather individuals staying to inherit the colony because the nest is a safe haven (see also Myles 1988). From there, the evolution of soldiers rather than workers may have marked the initial transition to eusociality. Furthermore, it seems that intraspecific competition rather than predation pressure was the prime factor favoring the evolution of these soldiers.

7.6

Comparison with Cooperatively Breeding Vertebrates

The potential importance of the role of inheritance in the evolution of termite eusociality draws comparison with data from cooperatively breeding vertebrates. Here, the role of ecological factors has also been emphasized. The three most influential hypotheses to explain the evolution of helping behavior in vertebrates are: (a) ecological constraint hypothesis which argues that helping occurs because opportunities for independent breeding are limited or risky because of low availability of nesting sites or a high risk of mortality during dispersal (Emlen 1991, 1997); (b) life-history hypothesis that emphasizes that certain life-history characteristics of a species limit the opportunity for independent breeding (Arnold and Owens 1998); (c) benefit of philopatry hypothesis that stresses the long-term direct benefits of staying at the natal nest, such as inheritance of the natal territory (Stacey and Ligon 1991). In vertebrates, the life-history hypothesis seems to be most successful in explaining interspecific variation in the occurrence of cooperative breeding, while the ecological constraint hypothesis is strongly supported by intraspecific studies (Hatchwell and Komdeur 2000). Besides, however, several examples also show the importance of long-term direct benefits of nest inheritance (Heinsohn and Legge 1999). The termite studies support the benefit of philopatry hypothesis and the ecological constraints hypothesis, the latter however with restrictions (see below). According to the results for C. secundus, in wood-dwelling termites the opportunity of the workers to become neotenic replacement reproductives that inherit the nest seem to be the major driving force for staying at the nest as the opportunities for successful independent founding are difficult. Similar to some birds in which individuals stay at the nest and either do not help (Veltman 1989; Magrath and Whittingham 1997; Boland et al. 1997) or help, but raise unrelated offspring (Reyer et al. 1986; Dunn et al. 1995), C. secundus workers stay to gain direct fitness benefits. Why the termite workers do not work, although they would have the opportunity

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to help relatives and increase their inclusive fitness, could be explained by several factors, some of which are also proposed for the bird examples (Heinsohn and Legge 1999): (a) The costs of helping may be too high compared to the indirect benefit gains. Here a recently developed model provides interesting results (Jeon and Choe 2003). Totipotency delays the evolution of costly helping, as the costs in direct reproduction are high. This model’s predictions match with the findings in termites with altruistic helping occurring in MP species. (b) There might be no need to help (Heinsohn and Legge 1999). Probably this applies to wood-dwelling termites. They live inside their food, so costly foraging and food provisioning is not necessary. Being hemimetabolous insects, the young instars are quite independent and do not need to be cared for, except for infestation with gut symbionts which is not costly. Similarly in some cooperatively breeding birds it has been shown that helping is associated with the need for help and that it can be a flexible response (Reyer and Westerterp 1985). A lack of need for help in wood-dwelling termites ultimately means a low benefit of helping and may explain why it is not evolutionary favored. (c) Under some conditions individuals may have to pay through helping in order to be allowed to stay at the nest (Kokko et al. 2002). This can be selected even if it is not optimal for the helpers to help, but when ‘pay to stay’ is better than not paying and leaving the nest. Such conditions occur when the nest is a very valuable resource and staying of individuals causes costs to the dominant breeders, especially when relatedness among helpers and breeders is low. In wood-dwelling termites this would be the case for fused colonies in which unrelated individuals stay and consume the non-replenishable food resource. Yet, I do not have any indications that C. secundus workers have to pay under such conditions (Korb, unpubl. data). The ecological constraint hypothesis applies to C. secundus as well because dispersal is very costly. However, appropriate nest sites are not in limited supply. The stochasticity of the habitat (e.g., thunderstorms that suddenly and with a sufficient frequency create new patches of dead wood) prevents habitat saturation. Furthermore, in contrast to cooperatively breeding vertebrates, wood-dwelling termites have no opportunity to check the availability of nesting/breeding vacancies as they never leave the nest before the nuptial flight (Roisin 1994, 1999). Thus, perceived ecological constraints are constant for termites. Apart from these confinements, however, ecological constraints are important as they determine the costs of philopatry. Other factors being equal, if ecological constraints on founding a new colony are not very restrictive, then the benefits of philopatry need to be high to favor staying at the nest (Koenig et al. 1992; Kokko and Lundberg 2001). So the ecological constraints and the benefits of philopatry hypotheses reflect two sides of one coin. Hence, a combined approach that considers all factors is necessary to understand the evolution and maintenance of social life (Hatchwell and Komdeur 2000; Pen and Weissing 2000; Kokko and Ekman 2002). Such a unifying approach could be provided by reproductive skew theory, which aims to explain the extent to which reproduction is biased within animal societies by identifying the role of ecological, genetic, and social factors (Vehrencamp 1983; Reeve and Ratnieks 1993; Keller and Reeve 1994; Johnstone 2000). The tremendous development of skew theory

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has lead to many new models in recent years, but their relevance in nature still needs to be tested.

7.7

Conclusions

Ecological factors play a central role in the evolution of group nesting in termites as well as in vertebrates. This suggests that rarity of eusociality outside the insect world is not explained by differences in relatedness but rather the tendency to become eusocial might be linked to life-history traits that differ fundamentally between groups. Of course, however, this is not to say that relatedness, which is a requirement for altruism and eusociality, is not important. It simply means that differences in relatedness between different groups may not be the key factor in determining a predisposition to eusociality. To the extent that it resembles the wood-dwelling termites, the first step in the scenario for the evolution of termite eusociality was very similar to many cooperative breeding vertebrates. Ecological constraints and benefits of philopatry favor staying at the nest. One fundamental difference though is the larger group sizes in the termites. This may, therefore, represent a key prerequisite for the evolution of eusociality as a loss in direct reproduction can be offset by indirect fitness gains through: (a) defending a large group of relatives instead of few siblings; (b) helping to raise many siblings which is only possible if the mother has a high fecundity; (c) the occurrence of emergent properties that add further incentives for staying in the group (Fig. 7.5). Accordingly, two prerequisites, which birds and mammals usually lack, are necessary for the transition to eusociality: (a) a high fecundity and (b) large numbers of offspring that can stay at the nest and are not ‘forced’ to leave because there is no competition at the nest for food (no local resource competition) (Fig. 7.5). Under most conditions, offspring are selected to disperse from the nest to avoid competition among siblings (Hamilton and May 1977). Two mechanisms can overrule this: a high abundance of food at the nest that lasts reasonably long (i.e., for at least two generations that can co-exist) and/or high ecological constraints which make dispersal difficult. The latter is commonly included in many models on the evolution of sociality (e.g., see above ecological constraint hypothesis, reproductive skew models; Johnstone 2000), while the former is often only implicitly assumed. The comparison with termites, therefore, suggests that the general lack of eusociality in vertebrates might be because they can only achieve small families due to their low fecundity and the difficulty to have enough food to overcome local resource competition for more than two generations to coexist as individuals are large and rather long-lived compared to their food source (Fig. 7.5). Thus, the finally limiting trait accounting for the rarity of eusociality in birds and mammals would be their body size. Correspondingly, the only groups in which eusociality occurs are rodents, which are comparatively small mammals with a short generation time, high fecundity and long-lasting food sources (see Chap. 10).

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Transition to Eusociality

Opportunity to raise more siblings

(1)

(2)

High benefit to defend the nest

Emergent properties favor further increase of group size

Large Groups of Siblings

No Local Resource Competition

High Fecundity

(3)

(4)

Short Generation Time

Long - lasting Food Resource

Small Body Size

Fig. 7.5 Supposed life-history prerequisites for the evolution of eusociality. The transition to eusociality can only evolve if large groups of siblings can co-exist in the natal nest (1). However, for the co-existence of many individuals in large groups several life-history traits and conditions are necessary: high fecundity and a lack of local resource competition (2) which depends on a short generation time in relation to a long-lasting food source that provides enough food for at least two generations (3). All these traits link back to a small body size (4). In mammals and birds, their comparatively large body sizes cause low fecundity, long generation times and a high demand for food (the latter two resulting in local resource competition and dispersal from the natal nest) which prevents the occurrence of large groups of siblings, a necessary prerequisite for the transition to eusociality Acknowledgements I wish to thank K. Foster and J. Fields for helpful comments on the MS and improvements of the English. I gratefully acknowledge an Emmy Noether fellowship from the German Science Foundation (DFG, KO1895/2) and the Institute for Advanced Studies in Berlin for funding.

References Abe T (1987) Evolution of life types in termites. In: Kawano S, Connell JH, Hidaka T (eds) Evolution and coadaptation in biotic communities. University of Tokyo Press, Tokyo, pp 125–148

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Chapter 8

Kin-Recognition Mechanisms in Cooperative Breeding Systems: Ecological Causes and Behavioral Consequences of Variation Jan Komdeur(* ü ), David S. Richardson, and Ben Hatchwell

Abstract The idea that kin selection plays a key role in the evolution of helping behavior is supported by evidence that in many cooperatively breeding vertebrates, helpers assist relatives. However, whether help is directed towards kin through an active kin-selection process or whether it is merely the result of passive coincidence, i.e., because the helpers normally remain on the natal territory where the recipients of help just happen to be relatives has been a long-standing debate. Moreover, the nature and evolution of active kin-discrimination mechanisms that may be used within cooperative breeding (and how these are influenced by the ecology of the species) have, until recently, received little attention. In this review, we discuss the roles of indirect and direct kin-recognition mechanisms on effective kin discrimination, with kin recognition defined in its broader sense as the differential treatment of conspecifics according to their genetic relatedness. In cooperative breeding species, indirect recognition based on spatial rules that reliably predict relatedness can result in effective kin-directed helping. However, direct recognition based on environmental or genetic cues should be able to provide more discriminating mechanisms of kin recognition. Environmentally determined recognition cues and templates could provide an effective means of kin recognition because cooperative breeders are characterized by extended associations with family on stable territories, philopatry, and high adult longevity. Examples of long-term studies that have investigated the use of kin-recognition mechanisms in cooperative breeding vertebrate species are discussed. While there is strong evidence that kin-recognition cues and templates, especially based on vocalizations, can be learned during a period of association with kin, there is no evidence for the use of genetically determined recognition cues or templates. How the ecology of a species may determine the nature and accuracy of the kin recognition mechanism that evolves, and how this will in turn determine the limits of adaptive behavior, is discussed.

Jan Komdeur Animal Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, The Netherlands [email protected]

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Introduction

Cooperation is a ubiquitous feature of life. Individuals cooperate in hunting, feeding, fending off enemies, and migrating from one site to another; many animals live and breed in colonies, and males and females cooperate in mating and/or caring for offspring (Wilson 1975; Dugatkin 1997). This widespread occurrence of apparently cooperative behavior among animals is paradoxical for evolutionary biologists as ever since Darwin (1859), the general expectation is that individual behavior will be selfish in order to promote individual fitness (Dawkins 1976; Maynard Smith and Szathmáry 1995). While many instances of apparent cooperation are explicable as the selfish motives of individuals, other forms of cooperation have proved far more problematic for evolutionary biologists. For example, in some species individuals live and breed in bisexual groups of three or more adults and share parental care at a single nest (Brown 1987; Stacey and Koenig 1990). Typically, such cooperative or communal breeding systems comprise family groups that live together on permanent, stable territories. Among vertebrates, cooperative breeding is found in at least 3% of bird and mammal species (Brown 1987; Arnold and Owens 1998) and in some fish species (Taborsky 1994). There is a particularly high frequency (19%) of cooperative breeding in oscine passerine species (Cockburn 2003), in Australian birds (Russell 1989; Arnold and Owens 1998), and in primate species (Chap. 11). But why do animals breed cooperatively? The evolution of the traditional vertebrate cooperative breeding system, in which a pair of breeding individuals is assisted by helpers, is usually viewed as a two-step process: First, the decision by grown offspring to delay dispersal and independent breeding by staying at home, and second, the decision, by those individuals who have stayed at home, to become helpers (Emlen 1982). The first step in this model is usually attributed to the existence of constraints on independent breeding (Emlen 1982; Arnold and Owens 1998, 1999; Hatchwell and Komdeur 2000). The second step envisages that individuals that have already delayed dispersal can gain a net fitness benefit by helping. If interacting individuals are genetically closely related, kin-directed helping behaviors may be favored by kin selection (Hamilton 1964). In many cooperatively breeding birds and mammals, helpers do direct their care towards relatives, which supports the hypothesis that kin selection may constitute a significant driving force in the evolution of cooperative breeding (Emlen 1997). If so, then for helpers the ability to discriminate between kin and non-kin, and between different classes of kin, will be important in maximizing their fitness. However, while it is true that animal altruists tend to be genetically related to the individuals they help, whether this is the result of active kin selection or merely a result of passive processes such as delaying dispersal and remaining with the natal territory or group, has been a long-standing debate among evolutionary biologists (Komdeur and Hatchwell 1999; Griffin and West 2003). There is evidence that some animals use sophisticated mechanisms (e.g., phenotypes, Petrie et al. 1999; Shorey et al. 2000; vocalizations, Sharp et al. 2005; odors, Mateo and Johnston 2000; Mateo 2006) to discriminate between related and unrelated individuals. However, it could well be that environmental or ecological factors play a significant

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role as predictors of relatedness so that simple behavioral rules could offer an effective means of kin recognition. Note that in this chapter we use the term ‘kin recognition’ in the broad sense of Sherman et al. (1997) as the differential treatment of conspecifics differing in genetic relatedness; this definition makes no assumption about the mechanism or function of recognition, but simply defines it by the individuals that are the object of the behavior. What environmental factors are likely to be important in kin recognition? First, if recognition is learned during development, then a period of exclusive and prolonged association with relatives may facilitate such learning. Typical cooperative breeding systems where helpers assist with raising subsequent broods on their natal territory (Brown 1987) are characterized by an extended period of association with kin on the natal territory, stable and strong natal philopatry, limited access to breeding sites, and the presence of long-lived individuals (Stacey and Koenig 1990; Emlen 1991; Arnold and Owens 1998; Hatchwell and Komdeur 2000). In most cases, kin-directed helping precedes dispersal and independent breeding. In such situations, a decision rule ‘care for any offspring in my natal territory’ could serve as a reliable discriminator between kin and non-kin. Furthermore, the long period of extended care may allow the helper to develop a simple rule of thumb such as ‘help anyone who fed me as a nestling’, which may be a good predictor of relatedness. Second, variation in territory quality and level of habitat saturation in which cooperative breeders live may also play a role in kin discrimination rules. For example, prolonged associations with kin may occur when ecological factors cause dispersal costs to be high (Emlen 1994). Consequently, it may be the degree of variation in dispersal costs that sets the scene for the development and accuracy of kin recognition cues. The recent advent of powerful molecular genotyping techniques now allows us to determine parentage and relatedness within complex cooperative breeding systems, and also to gain a much more detailed understanding of the dispersal behavior of individuals and its consequences for the genetic architecture of populations. Furthermore, many studies of cooperatively breeding animals are sufficiently long-term that pedigrees can be determined and the lifetime reproductive success of individuals can be quantified precisely. Therefore, not only are we able to investigate kin-directed care and potential recognition mechanisms using field observations and experiments, but, in principle, we should be able to determine the direct and indirect fitness benefits accruing to subordinates and breeding parents within cooperatively breeding species (Stacey and Koenig 1990; Cockburn 1998; Richardson et al. 2002; Dickinson and Hatchwell 2004). Consequently, we are now in a position to determine the role ecological factors play in shaping such cooperative breeding systems. The aims of this review are first to discuss the role of kin selection and hence the potential importance of effective kin recognition in cooperatively breeding animals and, secondly, to consider the influence of environmental factors in determining the mechanism of recognition that provides effective kin discrimination. We will concentrate specifically upon cooperatively breeding vertebrates as the potential importance of kin selection in this group is still much debated (Cockburn 1998; Clutton-Brock 2002; Griffin and West 2003). We begin with a general outline of

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kin-selection theory in which we review the studies that have used parentage analyses to determine the indirect fitness benefits gained by subordinates and the potential for kin selection to mediate cooperative breeding. We then present studies that have investigated the mechanism through which kin discrimination works and the likely impact of ecology or environment. Lastly, we outline some of the unresolved issues within this field and suggest future research objectives.

8.2

Kin-Selection Theory

At first sight, investing resources into non-descendant offspring appears contradictory to the aim of maximizing one’s own genetic contribution to future generations, but this paradox can usually be resolved by studying the costs and benefits of alloparental care for the donors as well as for the recipients. Individuals could be expected to behave altruistically if the marginal gain in fitness via their relatives was greater than their own personal loss (Hamilton 1964; Maynard Smith 1964). Alloparental care will thus be favored if Rb − c > 0, where R is the genetic relatedness between the helper and the offspring helped, b is the fitness benefit to the offspring helped, and c is the fitness cost of helping (Hamilton 1964). Hamilton’s rule predicts that the level of kin discrimination would also be expected to vary with the cost (c) or benefit (b) of helping. Kin discrimination will be favored most when the costs and the benefits of helping are high. Alloparents may accrue indirect fitness benefits through the increased productivity of their relatives’ current brood, the increased survival of recipient young, and through increased parental survival or future breeding success (Brown 1980; Mumme et al. 1989; for reviews, see Brown 1987; Emlen 1991; Cockburn 1998; Clutton-Brock 2002; Roulin 2002; Koenig and Dickinson 2004). These indirect, or kin-selected, benefits are widely regarded as being of fundamental importance in the evolution of cooperative breeding systems (Brown 1987; Emlen 1997), but such benefits can be accrued only if helpers assist their relatives. Furthermore, helpers can accrue the largest indirect fitness gains by providing aid to the closest genetic relatives (‘kin discrimination’; Stacey and Koenig 1990). As a consequence, the ability to discriminate between individuals, or groups of individuals, and to assess the relatedness of social partners has been suggested to play a major role in the evolution of social behavior (Komdeur and Hatchwell 1999). Only by responding differently to kin and non-kin can an individual maximize the fitness benefits delineated by inclusive fitness. Individuals should, therefore, possess some mechanism or rules for identifying their kin and assessing their relatedness to social partners.

8.3

Evidence for Kin-Directed Care in Social Systems

The most widely employed means of testing whether kin selection is important in the evolution or maintenance of a specific cooperative breeding system is to determine whether the probability, or amount, of helping covaries with the degree of

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genetic relatedness between potential helpers and beneficiaries—helpers should preferentially aid closer relatives. Such kin-directed behavior and care have been demonstrated empirically across a range of social animals (Emlen 1995; Komdeur and Hatchwell 1999; Koenig and Dickinson 2004). When faced with a choice of potential recipient nests, helpers preferentially help the breeding pair to whom they are most closely related in the white-fronted bee-eater (Merops bullockoides; Emlen and Wrege 1988), Galápagos mockingbird (Nesomimus parvulus; Curry 1988), bell miner (Manorina melanophrys; Clarke 1984, 1989; Painter et al. 2000), pinyon jay (Gymnorhinus cyanocephalus; Marzluff and Balda 1990), western bluebird (Sialia mexicana; Dickinson et al. 1996), and long-tailed tit (Aegithalos caudatus; Russell and Hatchwell 2001) (Table 8.1). The ability of individuals to recognize varying degrees of kinship (relatedness) is also expected to vary in different social systems (Pusey and Wolf 1996). The indirect fitness benefits available to helpers will be relatively low when helping half-sibs (produced by a parent plus unrelated step-parent) rather than full-sibs, so care by helpers is predicted to be reduced. White-fronted bee-eaters (Emlen 1997), Florida scrub jays (Aphelocoma coerulescens; Mumme 1992), and Seychelles warblers (Acrocephalus sechellensis;

Table 8.1 Observational and experimental evidence for kin-directed care and the cues used to assess kinship in vertebrate social systems Species Facultative adjustment of helping towards close kin Observational evidence: White fronted bee-eater (Merops bullockoides) Bell miner (Manorina malanophrys) Pinyon jay (Gymnorhinus cyamocephalus) Western blue-bird (Sialia mexicana) Florida scrub jay (Apholecoma coerulescens) Seychelles warbler (Acrocephalus sechellensis)

Long-tailed tit (Aegithalos caudatus)

Experimental evidence: Galápagos mockingbird (Nesomimus parvulus) Seychelles warbler

Cue

Source

Association with parents

Emlen and Wrege 1988; Emlen 1997 Clarke 1984, 1989, Painter et al. 2000 Marzluff and Balda 1990 Dickinson et al. 1996

Association with parents Association with parents Association with both parents Association with mother Association with kin

Association with parents Association with mother

Mumme 1992 Komdeur 1994 Richardson et al. 2003a, 2003b Hatchwell et al. 2001a, Russell and Hatchwell 2001 Curry 1988 Komdeur et al. 2004 (continued)

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Table 8.1 (continued) Species

Cue

Source

Long-tailed tit

Adults call

Sharp et al. 2005

No facultative adjustment of helping towards close kin: Galápagos hawk (Buteo galapagoensis) Superb fairy-wren (Malurus cyaneus) Mexican jay (Aphelocoma ultramarine) Green woodhoopoe (Phoeniculus purpureus) Stripe-backed wren (Campylorynchus nuchalis) Red-cockaded woodpecker (Picoides borealis) Meerkat (Suricata suricatta)

Delay et al. 1996 Dunn et al. 1995 Brown and Brown 1990 DuPlessis 1993 Rabenold 1985; Piper 1994 Walters 1990 Clutton-Brock et al. 2000, 2001 Rasa 1977, 1986

Dwarf mongoose (Helgale parvula) Facultative adjustment of helping towards unrelated individuals White-browed scrubwren (Sericornis frontalis)

Pied kingfisher (Ceryle rudis rudis) Rifleman (Acanthisitta chloris) White-winged chough (Corcorax melanorhamphos) Dwarf mongoose (Helogale parvula) Lake Tanganyika cichlid (Neolamprologus pulcher) African wild dog (Lycaon pictus)

Association with absence of mother

Magrath and Whittingham 1997; Whittingham et al. 1997 Reyer 1980 Sherley 1990 Heinsohn 1991 Rood 1990 Stiver et al. 2004 Creel and Creel 2002

Komdeur 1994; Richardson et al. 2003a, 2003b) all exhibit the predicted adjustment in helping behavior. Each study found that the proportion of non-breeders that helped decreased when unrelated step-parents became breeders. Although the species studied above provide support for the facultative adjustment of helping by subordinates towards close kin, in studies of a suite of other species including the Galápagos hawk (Buteo galapagoensis; Delay et al. 1996), superb fairy-wren (Malurus cyaneus; Dunn et al. 1995), Mexican jay (Aphelocoma ultramarine; Brown and Brown 1990), green woodhoopoe (Phoeniculus purpureus; DuPlessis 1993), stripe-backed wren (Campylorynchus nuchalis; Rabenold 1985; Piper 1994), red-cockaded woodpecker (Picoides borealis; Walters 1990), meerkat (Suricata suricatta; Clutton-Brock et al. 2000, 2001) and dwarf mongoose (Helogale parvula; Rasa 1977, 1986) helping behavior was not found to co-vary with relatedness (Table 8.1). However, a frequently overlooked point is that within a species, the absence of a correlation between helping and relatedness is not sufficient to reject an inclusive fitness

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argument that invokes kin selection as the evolutionary route to cooperative breeding. Indiscriminate helping could still return an indirect fitness benefit, providing that young are, on average, commonly related to the helpers, as certainly occurs in some of the species listed above, because of, for example, strong natal philopatry. A stronger case for rejection of kin selection is provided by cases where helpers are unrelated to the adults they help, or where helping is preferentially directed to broods to which the helpers are unrelated. For example, alloparents in white-browed scrubwren (Sericornis frontalis; Magrath and Whittingham 1997; Whittingham et al. 1997), pied kingfisher (Ceryle rudis rudis; Reyer 1980), rifleman (Acanthisitta chloris; Sherley 1990), white-winged chough (Corcorax melanorhamphos; Heinsohn 1991), dwarf mongoose (Rood 1990), Lake Tanganyika cichlid (Neolamprologus pulcher; Stiver et al. 2004), and African wild dog (Lycaon pictus; Creel and Creel 2002) all prefer to help unrelated dominants (Table 8.1). However, there is the question of how generalizable are reported directed care patterns. This is exemplified in a study on dwarf mongooses. One study reported no association between helping and relatedness of the brood (Rasa 1977, 1986), whereas a later study found helpers preferentially helping unrelated broods (Rood 1999). These considerations lead to the conclusion that even if kin selection does provide a general explanation for cooperative breeding in vertebrates, one would expect to see variation in the degree of kin discrimination and of kin-recognition mechanism among species. This variation could reasonably be expected to run from extremes of sophisticated recognition and discriminatory mechanisms through to indiscriminate helping. The challenge for researchers interested in social evolution is to identify the factors that determine where a species or population is likely to lie along this continuum.

8.4

Principles of Kin Recognition

Despite the wealth of research examining whether individuals can recognize one another (Fletcher and Michener 1987; Hepper 1991) little research has been conducted on the underlying mechanisms, or proximate causes, of kin recognition. In cooperatively breeding species, subordinates and breeders could potentially assess kinship using various phenotypic or spatial cues (reviewed in Komdeur and Hatchwell 1999; Koenig and Haydock 2004). First, individuals might recognize as a relative any conspecific encountered in a location that predictably contains only kin (e.g., a nest or territory). Such site-specific behavior results in ‘indirect recognition ’ where the cue is not a property of the recipient per se, but rather its location in space. The alternative is that recognition is based on some property of the recognized individual rather than simply its location. This recognition system requires an actor and a recipient and can be divided conceptually into three components: production, perception, and action (Reeve 1989; Gamboa et al. 1991; Sherman et al. 1997). The production component is the development of a phenotype in the recipient that can reliably signal genetic relatedness. Such phenotypic cues to kinship may

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exist in any sensory modality (Halpin 1991) and they may provide information that is individual-specific, or family- or group-specific, as in the colony odors of social insects (e.g., Breed and Bennett 1987). These kin-recognition cues may be acquired genetically or environmentally, or have components that are both inherited and learned. The perception component involves the development of recognition templates by the actor against which the phenotype of potential recipients can be compared. Again, such templates may be environmentally or genetically determined. However, there are few clear examples of genetically encoded templates (Keller and Ross 1998), and it seems likely that templates are usually formed through a learning process when encounters with relatives are frequent or predictable. Finally, the action component involves a response by the actor towards the recipient that will depend on the similarity between the cue and the template. In such actions, the actor may make one of two kinds of error: accepting non-kin as kin and/or rejecting kin as non-kin. The balance between acceptance and rejection errors will depend on the position of the acceptance threshold, which is likely to vary according to the nature of the production and perception components and to the relative costs and benefits of the action concerned (Reeve 1989; Sherman et al. 1997). One goal for studies of the mechanism of kin recognition in cooperative breeding systems is to determine what phenotypic cues are used for recognition and whether those cues and the actor’s recognition template are determined environmentally or genetically. A second major goal is to determine the accuracy of this recognition system and the resolution it gives in discriminating kin from non-kin, and different degrees of kinship among relatives. This latter issue is of fundamental importance for our understanding of the limits of adaptive behavior. Both goals are heavily dependent on an understanding of the environmental and life-history circumstances in which the recognition system has evolved.

8.5

Kin Recognition – the Role of Environmental Factors

Birds communicate routinely using both vocal and visual signals, but vocal cues have the advantage that they can be perceived over relatively long distances and in dense habitat. Vocalizations may also be fixed through an individual’s life-time, often following a relatively short learning period early in life. In contrast, visual signals may be unreliable because of regular molts, feather wear and age-related plumage variation. Therefore, it is not surprising that vocalizations are the most widespread recognition cues in birds (Halpin 1991) and have been shown to be important in recognition between mates (Speirs and Davis 1991; Wiley et al. 1991; Robertson 1996), parents and offspring (Beecher et al. 1981; Jouventin et al. 1999), siblings (Nakagawa and Waas 2004) and flock members (Nowicki 1983; Wanker et al. 1998; Vehrencamp et al. 2003). Vocal discrimination has been shown in some cooperative breeders (Payne et al. 1988, 1991; Price 1999), but until recently the

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mechanism underlying recognition has not been well understood for any species (Komdeur and Hatchwell 1999). As stated in the introduction, cooperative breeders are normally characterized by certain ecological and life-history traits: long family associations on stable territories, philopatry, and high adult longevity. Furthermore, in most cases, kin recognition is most important in the context of helping, and this behavior generally precedes dispersal and independent breeding. Therefore, in principle, indirect or environmentally determined recognition cues and templates could provide an effective means of kin recognition that would be expected to correlate closely with kinship. Indeed, current evidence does suggest that learning through association is the most likely mechanism of kin discrimination in vertebrate societies (Table 8.1). However, other behavioral, ecological, or life-history traits may act to reduce the effectiveness or reliability of an environmentally acquired recognition system. First, the longer helpers remain on their natal territory the higher the probability that there will be some turnover of breeders and, consequently, a reduction in their relatedness to the helped brood. In theory, recognition through association avoids this problem, provided that breeder turnover occurs after a putative ‘learning period’. Secondly, shared parentage of broods and extra-pair parentage occurs in many cooperatively breeding species (Cockburn 2004). This may not have a major impact on a helper’s relatedness to the brood provided that parentage is shared among its relatives within the social group, as in acorn woodpeckers (Melanerpes formicivorus; Haydock et al. 2001). But, in those cases where parentage (usually paternity) is attributable to non-kin from outside the social group, a helper’s kinship to the helped brood may be substantially reduced, e.g., superb fairy-wrens (Double and Cockburn 2003), Seychelles warblers (Richardson et al. 2002). In such cases, a helper may have few cues to its true relatedness to a brood. Two recent studies illustrate the use of kin-recognition cues acquired through association. In the Seychelles warbler, breeding pairs normally remain together within a territory as long as both birds survive, and offspring have a long period of dependence, remaining on the natal territory for at least 1 year (Komdeur 1992). In this species, subordinates have been shown to incorporate information about breeder turnover and parentage when deciding whether to help so that they maximize indirect fitness by preferentially helping genetically related nestlings (Richardson et al. 2003a, 2003b). First, help is conditional on the continued presence of the primary female (but not the male) who previously fed the subordinate in the nest (Richardson et al. 2003a, 2003b). As the continued presence of the primary female reliably indicates relatedness to the nestling, this cue is effective in maximizing indirect benefits to subordinates. The fact that the primary male is not used as a cue is logical from an evolutionary point of view because the high frequency of female infidelity in this species (Richardson et al. 2001) means that subordinates are often unrelated to the primary male. Consequently, the continued presence of the primary male does not reliably indicate relatedness between the subordinate and the nestling (Richardson et al. 2003a, 2003b). A cross-fostering experiment was also conducted that produced nestlings that were unrelated to the primary female that raised them. When cross-fostered offspring were compared to

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control offspring, the probability of becoming a helper was associated only with the continued presence of the primary female for both groups, which strongly supported the idea that helping is based on associative-learning cues and not on the direct assessment of genetic relatedness (Komdeur et al. 2004). Thus, in the Seychelles warbler, help is based on the identity of parents rather than the direct recognition of relatedness to nestlings. In the Seychelles warbler the decision rules used by subordinates to discriminate effectively between related and unrelated broods are well understood, although the recognition cues concerned have not been investigated directly. In another cooperative breeder, the stripe-backed wren, family-specific vocalizations enable individuals to discriminate kin from non-kin, but it is not known whether these calls are determined genetically or learned from other family members during development (Price 1998, 1999). Similar discriminatory behavior using vocalizations has also been demonstrated in superb fairy wrens, but again the relative importance of environmental and genetic factors in cue or template development is unknown (Payne et al. 1988). Recent research on the cooperative breeding system of the long-tailed tit has investigated the mechanism underlying discrimination of this sort. Typical cooperative breeding species often have limited potential for investigation of kin discrimination or recognition because helpers, being philopatric offspring, have little opportunity to choose between kin and non-kin when making helping decisions. One alternative is to consider whether helpers change their behavior when their social circumstances change, as described above for the Seychelles warbler. Another option is to investigate helper choices when offered the simultaneous choice of recipients of variable relatedness. However, as it is rare for cooperative breeding species to live in groups where potential helpers have a choice of whom to help, few studies have been able to consider whether helpers show a kin preference in this context (but see Emlen and Wrege 1988; Lessels 1990). These circumstances are most likely to occur in those species where help is ‘redirected’ (Emlen 1982), i.e., where helpers are failed breeders who choose to help at another pair’s nest. In longtailed tits, all mature individuals try to breed independently each year, but if their breeding attempt fails, these failed breeders may help raise offspring at another nest (Glen and Perrins 1988; Hatchwell et al. 2004). Observations showed that helpers usually assist at the nest of a relative, and their help has a significant effect on nestling recruitment so that helpers accrue a substantial kin-selected indirect fitness benefit from their cooperation (Hatchwell et al. 2004; MacColl and Hatchwell 2004). However, as discussed above, an apparent kin preference could emerge simply by failed breeders becoming helpers at the closest available nest in a kin-structured population. In fact this is not the case; an active choice of kin was demonstrated in an experiment where the success of breeding attempts was manipulated to offer potential helpers (i.e., failed breeders) the choice between equidistant broods belonging to kin and those belonging to non-kin: helpers preferentially helped kin (Russell and Hatchwell 2001). Furthermore, playback experiments have shown that long-tailed tits can discriminate between kin and non-kin on the basis of their vocalizations (Hatchwell et al. 2001a; Sharp et al. 2005). The calls that provide cues for discrimination develop during the last few days of the nestling period and, as adults, calls are individually distinctive (Sharp and Hatchwell 2005, 2006). Moreover, the

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calls of siblings are more similar than those of non-siblings (Sharp and Hatchwell 2005). Partial cross-fostering of nestlings among unrelated broods showed that cross-fostered birds that survived to adulthood had calls that were more similar to their foster siblings and foster parents than to their true siblings reared apart or their true parents (Sharp et al. 2005). Thus the characteristics of calls that can be used as kin recognition cues are learned during development rather than being genetically determined. Furthermore, the recognition template must develop in a similar way because foster siblings did not discriminate between related and unrelated brood mates when deciding whom to help as adults (Hatchwell et al. 2001a). The use of kin-recognition cues and templates that are learned during an early stage of development may result in recognition errors if young birds interact with non-kin during the putative learning period or if social relationships do not reliably predict genetic relatedness. In the case of the long-tailed tit, both are unlikely because extra-pair paternity and brood parasitism are rare (Hatchwell et al. 2002) and offspring usually associate with kin for several months after fledging (Hatchwell et al. 2001b), long after calls develop (Sharp and Hatchwell 2006). The pattern of cooperation is broadly consistent with the proposed recognition mechanism because a large majority of helpers are known to have associated with the breeders whose brood they helped during the nestling phase, either as siblings or as a recipient or donor of care (Sharp et al. 2005). Thus, a long-tailed tit presumably perceives other members of the population as either kin (individuals with which they were closely associated and which are potential recipients or donors of help) or non-kin (all other birds). This learning mechanism is conservative in the sense that it includes as potential recipients of help a subset of kin within the population with whom the helper has been directly associated. However, it makes evolutionary sense for long-tailed tits to avoid acceptance errors because evidence suggest that helpers accrue indirect fitness benefits (i.e., by assisting kin) but not direct fitness benefits through their cooperation (McGowan et al. 2003; MacColl and Hatchwell 2004). Current evidence therefore suggests that among cooperative breeders, kin recognition is achieved through learning of the phenotypic cues of kin during a period of close association (Table 8.1). As yet, there is no evidence for genetically determined recognition cues or templates. Nevertheless, the detailed studies of Seychelles warblers and long-tailed tits show that species-specific differences in ecology and life history have selected for different decision rules when making helping decisions. In the following section we consider the implications of an environmentally determined kin-recognition mechanism for helping behavior.

8.6

Consequences of Learned Kin Recognition for Helping Behavior

Relatedness between group members will usually facilitate the evolution of cooperation (Hamilton 1963; Bourke 1997). Indeed the widespread observation that cooperation routinely occurs among relatives in social vertebrates (e.g., Stacey and Koenig 1990) led to the early acceptance of kin selection as a key factor in the

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evolution of cooperative breeding systems (Emlen 1995, 1997). However, recent reviews have concluded that the case for kin selection driving the evolution of cooperative breeding is not as strong as once considered (Cockburn 1998; CluttonBrock 2002). First, most social vertebrate groups consist of relatives and it is not clear that the degree of relatedness is consistently higher in cooperative breeders than in other species that live in stable groups but do not breed cooperatively (Hatchwell and Komdeur 2000; Clutton-Brock 2002). Second, the magnitude of indirect fitness benefits relative to direct fitness benefits may have been overestimated due to incorrect calculation of indirect fitness (Creel 1990), failure to recognize the inclusive fitness costs of competing with kin (West et al. 2002), the confounding effect of individual or territory quality (Cockburn 1998) and an underestimation of breeding by apparently non-reproductive ‘helpers’ (Richardson et al. 2001, 2002). Finally, in many vertebrate societies, the amount of help given does not vary with the relatedness of the helpers (e.g., Clutton-Brock et al. 1999, 2000; Dunn et al. 1995; DuPlessis 1993). Furthermore, in birds, unrelated helpers typically constitute less than 10%, but sometimes as many as 45%, of all helpers (reviewed in Stacey and Koenig 1990) and this phenomenon is difficult to explain. We agree that inter-specific comparisons have often proved inconclusive in identification of ecological or demographic differences between cooperative and non-cooperative species (Hatchwell and Komdeur 2000), and that measuring inclusive fitness poses many challenges. However, so far as the third criticism is concerned, we suggest that an understanding of the process of kin recognition is critical before deciding what level of kin discrimination would be expected in a given species. In the Seychelles warbler and long-tailed tit, and indeed probably in other cooperative species, the mechanism of kin recognition is based upon learned cues and/or templates through association. However, the outcome, in terms of helping behavior, is highly variable. In the Seychelles warbler, subordinates adjust their care according to their likely relatedness to a brood (Komdeur 1994; Richardson et al. 2003a, 2003b; Komdeur et al. 2004). Such facultative adjustment of helping is widespread among social vertebrates (Griffin and West 2003). In a meta-analysis, Griffin and West (2003) also showed that the preferential helping of relatives is more common in species where helping provides a greater benefit. However, even in the kinselected cooperative breeding system of long-tailed tits (Hatchwell and Sharp 2006), where helpers show clear kin discrimination when deciding whether to help or not (Russell and Hatchwell 2001), there is no evidence for facultative adjustment of care by helpers according to their relatedness to a brood, even though this varies quite markedly (Hatchwell and Sharp 2006). This failure to discriminate different degrees of kinship probably results from having a simple recognition rule that categorizes conspecifics as either related or non-related. The key point is that the absence of fine discrimination in effort cannot be used to infer that kin selection is unimportant. Nevertheless, an adaptive explanation is still required for those cooperative breeding societies where related subordinates do not help (Cockburn 1998), or where helpers are unrelated to the young but still invest as heavily as close relatives

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(Table 8.1). Such behavior could result from recognition errors, the acceptance threshold being set relatively high or low, respectively. However, in some cases, helpers actively compete for access to unrelated offspring, as shown in the meerkat (Clutton-Brock et al. 2000), the superb fairy-wren (Dunn et al. 1995) and the stripebacked wren (Magrath and Whittingham 1997) and this competition to feed unrelated young may result in adoption, involving recruitment and care of dependent young from another group. Adoption has been seen in the Florida scrub jay (Woolfenden and Fitzpatrick 1984), and the Arabian babbler (Turdoides squamiceps; Zahavi 1990). An extreme form of adoption, ‘kidnapping’, occurs when adults herd young from another territory into their own territory. This has been seen in the white-winged choughs (Heinsohn 1991). Adult ‘kidnappers’ fed the fledglings they adopted, and these young later become unrelated helpers in their new groups. Another oft-cited explanation for care being given by helpers to non-kin is that helpers may foster the formation of ‘social bonds’ with recipient young, bonds that later benefit the helper either by increasing the probability that the young will return the favor, or by promoting development of coalitions beneficial in competing for breeding positions (Ligon 1983; Emlen 1991; Emlen et al. 1991). For example, whitewinged choughs require helpers to reproduce successfully, selection may have favored kidnapping because the resulting ‘special bonds’ cause kidnapped young to help their kidnappers (Heinsohn 1991). Thus, by feeding unrelated offspring, helpers may parasitize a kin-recognition mechanism based on associative learning; the deceived offspring recognize those who care for them as kin and later help rear their provisioner’s offspring (the ‘kinship deceit hypothesis’; Connor and Curry 1995). An alternative hypothesis to explain why helpers might provision unrelated offspring is that helpers increase their own survival and future reproduction by cooperating with others (direct fitness gains). Direct fitness benefits may be gained through several routes that have been extensively reviewed (e.g., Brown 1987; Emlen 1991; Dickinson and Hatchwell 2004), so we do not consider the various possibilities any further here. The important point is that in situations where helpers gain some direct fitness through their cooperative behavior, the ability to recognize and discriminate kin from non-kin is not necessarily a prerequisite for the evolution of helping behavior. For example, in several societies, subordinates not only maintain social relationships and helping activities with members of their own group but also (temporarily) leave groups to join other unrelated groups nearby and become helpers there (Rood 1990; Creel and Creel 2002; Stiver et al. 2004). In such cases, the goal of helping may be the establishment of familiarity and social relationships with individuals from other territories (Croft et al. 2004). Subordinates use these neighboring groups’ territories as safe havens when the risk of staying in the home territory increases (Bergmüller et al. 2005), and may successfully migrate into other groups (Stiver et al. 2004). This suggests subordinates may be prepared to risk expulsion because other groups are available to disperse to, and they may strategically choose which groups to join and which breeders to help. If dominants gain fitness by accepting additional helpers, helpers might trade their helping contribution for being accepted in a territory that provides beneficial conditions (Bergmüller et al. 2005).

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Concluding Remarks

Overall, the evidence supports the idea that kin selection plays a key role in favoring helping behavior within cooperative vertebrates. Therefore, it is unsurprising that kin discrimination is apparent in at least some species. Studies of cooperatively breeding birds are all consistent with the idea that vocal kin recognition cues and templates are acquired environmentally in a period of association with kin. This mechanism has the disadvantage that it is prone to acceptance errors if association with non-kin occurs during the putative learning period, and it may also mean that individuals fail to recognize conspecifics that may be close kin but with which there was no association during the crucial phase of development. However, an obvious conclusion is that the extent or accuracy of discrimination by helpers will be directly affected by the probability of such errors, so that the recognition mechanism will be important in determining the limits of adaptive behavior. There is abundant opportunity for investigating this idea both within and between species. Furthermore, in this chapter we have focused on social vertebrate species only, however, in order to understand the common principles of kin recognition in social animals, it is important to compare social vertebrate and invertebrate species with respect to the occurrence and mechanisms of kin discrimination. For example, in social insects there is not a single unambiguous example of true kin discrimination, based on true relatedness, and instead it seems that common odors, based on environmental cues, are used as an indicator of relatedness (e.g., Breed et al. 1994; Keller 1997; Holzer et al. 2006). The second conclusion is that selection for an effective kin recognition mechanism will depend on the importance of kin selection in the evolution of a particular species’ cooperative system. No kin discrimination is expected if the only benefit of helping is to increase the helper’s direct fitness, and the acceptance threshold for kin recognition would be expected to become more stringent as the relative importance of indirect fitness benefits increases, as found by Griffin and West (2003). Finally, we have discussed kin recognition only in the context of helping behavior and the role of kin selection, but kin recognition may also be very important for incest avoidance in kin-structured population if inbreeding depression is likely to have a significant effect on fitness (Koenig and Haydock 2004). A strategy of sex-biased dispersal may be generally effective in reducing the probability of close inbreeding, but other commonly observed behaviors within groups of social vertebrates such as forced eviction from or abdication of reproductive position, reproductive suppression and extra-group mating all require kin recognition. The intensity of selection for an effective kin-recognition system would be expected to depend on the probability and cost of incestuous pairing. Acknowledgments We are grateful to Judith Korb and Jürgen Heinze for the invitation to write this review. Furthermore, we thank them as well as an anonymous reviewer for providing valuable comments on this review.

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Chapter 9

Social Ecology of Horses Konstanze Krueger

Abstract Horses (Equidae) are believed to clearly demonstrate the links between ecology and social organization. Their social cognitive abilities enable them to succeed in many different environments, including those provided for them by humans, or the ones domestic horses encounter when escaping from their human care takers. Living in groups takes different shapes in equids. Their aggregation and group cohesion can be explained by Hamilton’s selfish herd theory. However, when an individual joins and to which group it joins appears to be an active individual decision depending on predation pressure, intra group harassment and resource availability. The latest research concerning the social knowledge horses display in eavesdropping experiments affirms the need for an extension of simple herd concepts in horses for a cognitive component. Horses obviously realize the social composition of their group and determine their own position in it. The horses exceedingly flexible social behavior demands for explanations about the cognitive mechanisms, which allow them to make individual decisions. “Ecology conditions like those that favour the evolution of open behavioural programs sometimes also favour the evolution of the beginnings of consciousness, by favouring conscious choice. Or in other words, consciousness originates with the choice that are left open by open behavioural programs.” Popper (1977)

9.1

Introduction

Horses (Equidae) are believed to clearly demonstrate the links between ecology and social organization (Berger 1977; Moehlmann 2002). Their social cognitive abilities enable them to succeed in many different environments, including those

Konstanze Krueger University of Regensburg, Department Biology I, Zoology, Universitätsstraße 31, 93053 Regensburg, Germany [email protected]

J. Korb and J. Heinze (eds.), Ecology of Social Evolution. © Springer-Verlag Berlin Heidelberg 2008

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provided for them by humans, or the ones domestic horses encounter when escaping from their human caretakers. Since horses show a strong tendency to live in groups, it seems to be reasonable to apply Hamilton’s selfish herd theory (1971) to herd aggregation and group cohesion in equids. According to Hamilton (1971), a new mutation, which increases its fitness by taking cover between conspecifics, can spread through the population and lead to herd aggregation, finally resulting in a better protection from predation for the individual herd members. Simple selfish movement rules thus can decrease predation risk when the predator attacks from outside the flock. Indeed, Viscido et al. (2001) found that, regardless of the predator’s size and speed, the risk of predation always decreases as long as the individuals take their mates into account. However, the individual movement rules required by Hamilton’s theory (1971) are too complex for most animals to follow. Viscido et al. (2002) called this phenomenon the “dilemma of the selfish herd”. In their opinion, the animal’s ability to detect its neighbors is an important factor in the dynamics of group formation. Not only the nearest neighbors but also the behavior of distant neighbors mediates information in case of predation. Reluga and Viscido (2005) suggested that predation-based selection can even increase the influence of distant neighbors relative to near neighbors. The concept of a “limited domain of danger” (James et al. 2004) suggests either a limited detection range or a limited attack range of predators. An analysis of individual movement rules showed that animals escape from danger best when they use a time minimization strategy rather than a nearest neighbor strategy. The aggregation and group cohesion of horses can presumably in part be explained by Hamilton’s selfish herd theory (1971). However, when an individual joins and to which group it joins appears to depend on individual decision based on predation pressure, intra-group harassment, and resource availability. For greater foraging efficiency, horses have to decide when to spread out, which comes at a cost of greater predation risk (Janson 1990). The social lives of equid herds can be compared to the fission-fusion model (Dyer 2000) of other social mammals. Like groups of apes (Dyer 2000), elephants (Moss and Poole 1983), and dolphins (Connor et al. 2000) they frequently split and reunite again. The social groups of most equids are much more stable, even though stallions may change their reproductive strategy and therefore their social affiliation several times throughout their lives. In contrast, mares tend to stay with the group they once joined after having departed from their natal group in their first estrus. Depending on predation pressure and resource availability they sometimes change their affiliation to a certain social group even later in life. Though these phenomena are probably best known from feral horses (Equus ferus caballus) they have to be discussed in the context of the whole equid family. Living in groups takes different shapes in equids. For species that live in wide grasslands, such as the Serengeti Plain of Tanzania or the valleys of Hustai National Park in Mongolia (King and Gurnell 2005), food and water resources are sufficient enough to allow females to feed together and to thus form stable groups, which consist of one or more mares, their offspring and usually one, but occasionally up to five males (Tyler 1972; Berger 1977; Moehlmann 2002). Such a system is

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referred to as “harem”, “family,” or “band.” Surplus stallions gather in separate bachelor groups that differ in size from two to approximately 17 horses (Berger 1977). Many bands form a structured social unit, called “herd,” which shows the same migration patterns within a common home range (Miller 1979). Berger (1977) observed a herd of more then 210 feral horses grazing, clustered in groups. Harem groups are common in Plains and Mountain zebra (Equus burchelli and E. zebra), Przewalski’s horses (E. ferus przewalskii), and feral horses (E. ferus caballus) and provide a relatively safe environment, as stable groups and the presence of a stallion help to fend off predators, such as wolves, lions, and hyenas. Mature females of a band often remain together throughout their whole lives, while stallions may change their reproductive strategy several times, depending on their age and fighting ability and the number of competitors they have to contend with (Feh 1999). Foals born into a group stay with it for 1–5 years before they dispers e (Moehlmann 2002). Young females usually leave during their first estrus and join other families (Berger 1986). Young males tend to stay for several more years before they depart to find bachelor groups (Moehlmann 2002) or found a harem of their own. According to Klingel (1972), in the absence of “playmates” male offspring disperses earlier from their natal group. While Berger (1986) could not find any correlation between dispersal age and number of peers in the feral horses of the “Great Basin” of the Western USA, Rutberg and Keiper (1993) could prove a strong correlation for male offspring dispersal age and the presence of playmates in Assateague Island ponies, Maryland. On average male offspring dispersed earlier than female offspring on Assateague Island. When food biomass levels drop below 40 g/m2 during periods of drought, normally stable groups of plains zebras may become unstable (Ginsberg 1988). This suggests that the stability of group and group size in equids is bound to the distribution and availability of resources. Especially in dry environments, such as the Danakil Desert of Ethiopia and Eritrea, the scattered supply of food and limited water usually does not permit females to forage close to one another and to form stable groups. Instead, males establish territories near critical sources of water or food, and control matings with all females, which come into the territory to drink or feed (Moehlmann 2002). African wild asses (E. africanus), feral asses (E. asinus), Grevy’s zebra (E. grevyi) and Asiatic wild asses (E. hemionus) organize themselves without permanent bonds between adults, although they sometimes form temporary groups. Stallions of these species can dominate their territories for years. They may tolerate other males in this area but monopolize mating. Controlling access to water is critical. Lactating females need to drink at least once a day, and so they will stay as close to a pond or stream as possible. A female comes into estrus a week or two after giving birth and, if she is not then fertilized, again about a month later. Thus, the territorial male has several chances to father a new foal. The females, in turn, do not only gain access to water, but may also benefit from reduced harassment from bachelor males and better protection from predators (Klingel 1977; Moehlmann 2002).

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Ecology and Social Organization of Feral Horses

According to genetic data, horses, E. caballus, were domesticated repeatedly from several distinct populations of wild horses (Jansen et al. 2002). Today, all domestic and feral horses are organized in social groups. For a full understanding of the evolutionary roots of their social behavior, a comparison with their wild ancestors would be of immense value. Unfortunately, Przewalski’s horses, the last representatives of wild horses, are now declared to be extinct in their native habitats (Klimov and Orlov 1982). Those that still exist are descendants of 11 breeding animals, which themselves are descendants of 39 horses caught in the field and brought into European zoos between 1899 and 1902, plus one mare captured in Mongolia as a foal in 1947 (Ryder and Wedemeyer 1982). Almost nothing is known on their behavior in native habitats. Today they are kept in zoos (Kolter and Zimmermann 1988), in semi-wild reserves (Feh 1988), or reintroduced into the wild, for instance in the Hustai National Park, Mongolia (King and Gurnell 2005), where they form stable harem-type groups. It remains unclear, however, whether inbreeding has affected the behavior of Przewalski’s horses and whether behavioral characteristics found in domestic and feral horses but not in Przewalski’s horses, arose as a result of genetic drift, adaptation, or domestication (Berger 1986). More insight in the “natural” behavior and social organization of domestic horses comes from the study of free-ranging populations of feral horses. Ever since horses have been domesticated 2,500–5,000 years ago (Clutton-Brock 1981) they have escaped from their caretakers and organized themselves in freeranging groups. The process of feralization can be considered successful if the escapees form stable populations, fare well, and reproduce. Stable populations of feral horses exist on islands off the North American Atlantic coast (Welsh 1975; Keiper 1979; Rubenstein 1981), in subhumid and arid plains of continental Australia (McKnight 1976), deserts and mountains of western North America (Salter and Hudson 1982; Miller and Denniston 1979; Berger 1977), and the North Island of New Zealand (Cameron et al. 2003). Semi-wild populations are still managed in England’s New Forest (Tyler 1972; Pollock 1980) and Exmoor preserves (Gates 1979), as well as in the Camargue Delta in France (Duncan 1980; v. Goldschmidt and Tschanz 1978; Feh 1999). Feral horses form harem-type social organizations, usually consisting of one, in some cases up to five stallions, in which usually only the alpha and the beta stallion reproduce (Linklater et al. 1999; Feh 1999), and several mares and their offspring, which stay in the harem until maturity. Until now, the existence of single male bands and multiple male bands has not been sufficiently explained (Linklater and Cameron 2000; Feh 2001). The latter tend to be larger in group size and are consistently more stable than single male bands (Miller 1979). Female offspring eventually disperses to other harems, whereas male offspring form bachelor groups. Stallions usually change between different reproductive

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strategies, such as holding a harem, joining a bachelor group, or occasional sneak mating several times throughout their lives (Miller 1979; Feh 1999). Migrating females may join other bands or bachelor stallions (Berger 1986).

9.3

Environmental Influences on the Group Size of Feral Horses

Along with primates, group-living ungulates are believed to show the best correlation between body size, ecology and social organization. In general, species that exploit open environments tend to be larger in size and more gregarious than those who live in limited habitats abundantly covered with vegetation. Body size is affected by food distribution and foraging locations, and at the same time has consequences on anti-predatory behavior and spatial distribution patterns (Eisenberg 1981; Geist 1978). According to Waring (1979), the social organization of horses is strongly affected by the distribution of resources and individual distribution in space. Groups tend to be larger in size in open environments than in bordered habitats, especially when resources are abundant. However, environmental stress such as severe weather conditions in winter as well as food limitation during dry seasons causes bands to split into smaller groups (Miller 1979), which then usually roam on vast, overlapping areas (Salter 1979). In contrast, in island habitats with limited dispersal, high frequencies of interactions, and evenly distributed resources, feral horse herds have been observed to live in non-overlapping home ranges (Zervanos and Keiper 1979) or to become territorial and repel intruding horses (Rubenstein 1978). Parasites also appear to have a strong influence on group size at least in Camargue horses, for which Duncan and Vigne (1979) found a positive correlation between group size and the rate of attack by blood sucking flies. The per capita rate of bites was lower when horses gathered in large groups than in small ones. Feral horses are challenged by only a few effective predators, and reports on predation by wolves, lions and bears are anecdotal (Berger 1986). Humans, however, have a strong impact on group size and stability. The increase of the population size of feral horses in North America requires regulation by removal or translocation (U.S. Bureau of Land Management 2006). Such disruptions have a severe influence on the behavioral stability and the group size of herds as well as the well-being of the horses. For example, Tyler (1972) reported that group size in New Forest ponies, in which nearly all the colts and fillies are removed in autumn or winter remained small. On Sable Island, a chain of sand dunes in the North Atlantic Ocean, a new inexperienced male moved the herd into regions with poor shelter and poor food quality after the loss of a herd stallion in winter (Welsh 1975).

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The Ecology of Relationships in Horses

Groups of horses are structured by dominance hierarchies, however, the exact meaning and nature of such hierarchies are discussed (Berger 1977; Ellard and Cromwell-Davis 1989; Houpt et al. 1978; Houpt and Wolski 1980; v. GoldschmidtRothschild and Tschanz 1977; Heitor et al. 2006a, 2006b). Dominance relationships among domestic horses have been commonly investigated by paired feeding tests, an interaction contest over the limited resource “food”. However, Ellard and Cromwell-Davis (1989) mentioned that the results of such a test with draft-horse mares did not match their observations of the dominance hierarchy of the same horses in field. In recent studies, dominance relationships have been estimated by approach-retreat interactions and the direction of threats and submissive gestures (McDonnell and Haviland 1995; McDonnell 2003; Heitor et al. 2006a, 2006b), interactions that are thought to be correlated with the individual resource holding power (RHP) (Pusey and Packer 2003). In dyadic encounters, RHP is often a reliable predictor of the rank of interacting individuals. With increasing group size, it becomes less and less probable that dominance hierarchies are linear due to differences in RHP alone (Mesterton-Gibbons and Dugatkin 1995). Instead, the RHPs of animals for different resources are likely to overlap, as the value of different resources may vary between individuals and with time and situation. A hungrier animal, for example, would tolerate greater costs and thus fight longer and harder for food (e.g., Parker 1984; Houston and MacNamara 1988). In addition, dominance rank of horses appears to be correlated with age and the length of time the individual has resided in the group (Keiper and Sambraus 1985; Linklater et al. 1999), both of which are uncorrelated with RHP (Pusey and Packer 2003). For an alternative concept of dominance relationships in horses, which matches non-linearity due to overlapping RHPs, Goldschmidt-v. Rothschild and Tschanz (1978) proposed to divide social groups into three dominance groups. All horses classified as members of one level (A, B or C) interact with each other and may change their social position within their respective group, depending on the situation, but horses of level A generally are dominant over those of levels B and C, and horses of level B are dominant over those of level C, regardless of the context. Social status has also been discussed to be inherited. Houpt and Wolski (1980) investigated the social ranks that the offspring of ten thoroughbred mares obtain in their own age groups after weaning. The foals of high-ranking mares tended to obtain similar ranks as their mothers, while foals of mares of middle and low dominance rank were not consistently found in the same rank position. In addition, Feh (1999) reported that the sons of low-ranking and high-ranking mares in Camargue horses, obtained similar ranks as their mothers throughout their reproductive period. The proximate mechanisms leading to the heritability of social status are unclear. Individuals may learn by observing others as well as from their first few encounters with opponents (Huntingford and Turner 1987; Clutton-Brock and Parker 1995).

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The occurrence of successful sneak mating (Feh 1999; Linklater and Cameron 2000) relativizes the importance of RHP and dominance relationships for the reproductive success of male horses. Nevertheless, long-term paternity data show that dominant stallions, which hold single stallion bands, have a higher reproductive success than stallions pursuing other mating strategies. In multi-male bands, the dominant stallion can sire the largest percentage of foals, but up to one-third of matings can be ascribed to the beta stallion. “Sneak mating” has had the lowest success (Feh 1999; Linklater and Cameroon 2000). When separated from their herd companions, horses have a strong tendency to return to their social unit (e.g., Tyler 1972). Miller (1979) reported that male horses from bachelor groups or from other bands did not attempt to gain access to female horses that coincidently were separated from their group. In contrast, wandering females are commonly accepted by band leading or bachelor stallions (Berger 1986), but it is unknown how stallions realize that a mare is willing to be accompanied or integrated into a new group.

9.5

Cooperation and Alliances

Hierarchies in horse herds are complicated by the formation of alliances and cooperation among individuals. In addition to single-male bands, multiple-male bands exist (Miller 1979; Berger 1986; Feh 1999; Linklater et al. 1999), which tend to be larger in group size and consistently more stable (Miller 1979). This might be due to the existence of alliances among stallions (Feh 1999; Linklater et al. 1999; Feh 2001). In chimpanzees, alliances seem to destabilize dominance hierarchies but induce a state of mutual interdependence among individuals and lead to a greater access to resources (De Waal 1982; Nishida 1983). In multi-stallion bands of horses, the partners of dominant stallions are subordinate in rank. While the beta stallion has a higher reproductive success than subordinate stallions relying on “sneak mating,” the dominant stallions of such bands sire fewer foals than dominant stallions from single-stallion bands. Stallions, which join multi-stallion bands additionally to the alpha and the beta stallion, have been reported not to reproduce (Feh 1999; Linklater and Cameron 2000). The advantage for the dominant stallions comes from the higher success of multi-stallion bands to fend off rivals and to avoid sneak matings (Linklater and Cameron 2000) and foal mortality appears to be lower in multi- than in single-stallion bands (Duncan 1992; Feh 1999). In the studies of Feh (1999) and Duncans (1992), foal survival could still be linked with the foaling rate of the respective groups. However, Linklater et al. (1999) could not support this observation but instead found that foaling rate, as well as offspring mortality, was negatively correlated with the aggression rate stallions display towards their mares. In their studies, aggression rate was higher in multi-stallion groups than in single-stallion groups, which caused lower fecundity and a higher group travel rate in the mares. The latter directly correlated with offspring survival. In contrast, Miller (1979) found that multi-male groups were consistently more stable than single-male bands.

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Whether mares form alliances against stallions or other mares has as yet not been demonstrated, though mares play a much larger part in the social lives of horse herds than stallions do. Goldschmidt von Rothschild and Tschanz (1978) suggested additional alliances among members of rank groups A, B, and C. The occurrence of mutual grooming between stallions and mares was not correlated to their mating activities and independent of their individual ranks. Explanations of the patterns of social interactions and sexual affiliations are as yet unclear. Another behavioral pattern that might fit into the category “cooperation and alliances” is “interference” (McDonnell and Haviland 1995; McDonnell 2003). In interferences, stallions move in between pairs of fighting stallions and thus disrupt their combat. This behavior has been observed in horses, Przewalski’s horses (Keiper 1988), zebras (Schilder 1990) and Asiatic wild asses (Bannikov 1971).

9.6

Eavesdropping and Communicative Networks

In order to understand complex behavioral patterns such as cooperation and alliances, it is necessary to analyze social interactions on the level of the signals that individuals receive from their companions. Of particular interest is the behavior of uninvolved bystanders after eavesdropping on dyadic encounters among group members. It has recently been investigated what animals know about themselves and their social environment in fish, birds, and bats (McGregor 1993; Oliveira et al. 1998; Naguib et al. 1999; Dugatkin 2001; McGregor and Dablesteen 1996; Paz-y Miño 2004). For example, in Siamese fighting fish, bystanders were less aggressive towards the fish who had won a previous interaction observed by the bystander than towards the fish who lost (Oliveira et al. 1998). Horses appear to similarly observe their social environment and to utilize information they draw from monitoring interactions among others. This is suggested by the fact that severe fighting is very rare, especially in well-settled harems (Berger 1986), as well as in cases in which stallions did not attempt to gain female horses that coincidently were separated from their group (Miller 1979). It was recently shown that bystander horses adjust their response to an experimenter according to their own dominance relationship with the horse whose reaction to the experimenter they had observed before. In an experiment that used the “round-pen” technique of “horse-whisperers” (Rivera et al. 2002; Sighieri 2003; Miller and Lamb 2005; Krüger 2007), bystander horses immediately followed the experimenter after previously watching a dominant horse doing so but did not follow after observing a subordinate horse or a horse from another social group doing so (Krüger and Heinze subm.). The results of this study suggest social reasoning in inter-specific dominance relationships and for the first time document observational learning in horses.

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Conclusions

The latest research concerning social knowledge that horses display in eavesdropping experiments affirms the need for an extension of pure genetic herd concepts in horses for a cognitive component. Horses obviously realize the social composition of their group and are even able to determine their own position in it. The horses’ exceedingly flexible social behavior eagerly demands for explanations about the cognitive mechanisms, which allow horses to determine their individual decisions. As Nicol (2002) already claimed, there is an urgent need for specific research on horses’ cognitive abilities. Aside from basic cognitive research, especially, the assumption for the existence of alliances in horses (Feh 1999) needs to be evaluated more closely. Acknowledgements I thank Jürgen Heinze and Judith Korb for inviting me to write this chapter as well as for helpful comments on earlier versions of the manuscript. For the latter, as well as for help and advice in my literature research I thank Katherine Albro Houpt. Jon Seal improved the English. The study was supported by an HWP II grant of the University of Regensburg.

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Ellard M-E, Crowell-Davis SL (1989) Evaluating equine dominance in draft mares. Appl Anim Behav Sci 24:55–75 Feh C (1988) Social behaviour and relationships of Przewalski’s horses in Dutch semi-reserves. Appl Anim Behav 21:71–87 Feh C (1999) Alliances and reproductive success in Camargue stallions. Anim Behav 57:705–713 Feh C (2001) Alliances between stallions are more than just multimale groups: reply to Linklater and Cameron (2000) Anim Behav 61:F27–F30 Gates S (1979) A study of home ranges of free-ranging Exmoore ponies. Mamm Rev 9:3–18 Geist V (1978) Life strategies, human evolution, environmental design: toward a biological theory of health. Springer, Berlin Heidelberg New York Ginsberg JR (1988) Social organisation and mating strategies of an arid adapted equid: the Grevy’s zebra. PhD Thesis, Princeton University, Princeton, 268 pp Goldschmidt-Rothschild Bv, Tschanz B (1978) Soziale Organisation und Verhalten einer Jungtierherde beim Camargue-Pferd. Z Tierpsychol, pp 372–400 Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311 Heitor F, do Mar Oom M, Vicente L (2006a) Social relationships in a herd of Sorraia horses: Part I. Correlates of social dominance and contexts of aggression. Behav Proc 73:170–177; doi:10.1016/j.beproc.2006.05.004 Heitor F, do Mar Oom M, Vicente L (2006b) Part II. Factors affecting affiliative relationships and sexual behaviours. Behav Proc 73:231-239; doi:10.1016/j.beproc.2006.05.004 Houpt KA, Wolski TR (1980) Stability of equine hierarchies and the prevention of dominance related aggression. Equ Vet J 12:18–24 Houpt KA, Law K, Martinisi V (1978) Dominance hierarchies in domestic horses. Appl Anim Ethol 4:273–283 Houston AI, McNamara JM (1988) Fighting for food: a dynamic version of the Hawk–Dove game. Evol Ecol 2:51–64 Huntingford FA, Turner AK (1987) Animal conflict. Chapman & Hall, London James R, Bennett PG, Krause J (2004) Geometry for mutualistic and selfish herds: the limited domain of danger. J Theor Biol 228:107–113 Jansen T, Forster P, Levine MA, Oelke H, Hurles M, Renfrew C, Weber J. Olek K (2002) Mitochondrial DNA and the origins of the domestic horse. Proc Natl Acad Sci USA 99:10905–10910 Janson CH (1990) Social correlates of individual spatial choice in foraging groups of brown capuchin monkeys, Cebus paella. Anim Behav 40:910–21 Keiper RR (1979) Population dynamics of feral ponies. In: Denniston RH (ed) Symposium on the ecology and behaviour of wild and feral equids. University of Wyoming, Laramie, pp 175–184 Keiper RR (1988) Social interactions of the Przewalski horse (Equus przewalskii Poliakov, 1881) herd at the Munich zoo. Appl Anim Behav Sci 21:89–97 Keiper RR, Sambraus HH (1985) The stability of equine dominance hierarchies and the effects of kinship, proximity and foaling status on hierarchy rank. Appl Anim Behav Sci 16:121–130 King SRB, Gurnell J (2005) Habitat use and spatial dynamics of takhi introduced to Hustai National Park, Mongolia. Biol Cons 124:277–290 Klimov VV, Orlov VN (1982) Present state and problems of conservation of Equus przewalski. Soviet J Zool 61:1862–1869 Klingel H (1972) Social behaviour of African Equidae. Zool Afr 7:175–186 Klingel H (1977) Observation on social organization and behaviour of African and Asiatic wild asses (Equus africanus and E. hemionus). Z Tierpsychol 44:323–331 Kolter L, Zimmermann W (1988) Social behaviour of Przewalski horses (Equus p. prezewalskii) in the Cologne zoo and its consequences for management and housing. Appl Anim Behav Sci 21:117–145 Krueger K (2007) Behaviour of horses in the “Round pen technique.” Appl Anim Behav Sci 104:162–170

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Linklater WL, Cameron E (2000) Test for cooperative behaviour between stallions. Anim Behav 60:231–743 Linklater WL, Cameron EZ, Minot EO, Stafford KJ (1999) Stallion harassment and the mating system of horses. Anim Behav 58:295–306 McDonnell SM (2003) The equid ethogram: a practical field guide to horse behavior. Eclipse Press, Lexington, KT McDonnell SM, Haviland JCS (1995) Agonistic ethogram of the equid bachelor band. Appl Anim Behav Sci 43:147–188 McGregor PK (1993) Signalling in territorial systems: a context for individual identification, ranging and eavesdropping. Phil Trans R Soc B 340:237–244 McGregor PK, Dabelsteen T (1996) Communication networks. In: Kroodsma DE, Miller EH (eds) Ecology and evolution of acoustic communication in birds. Cornell University Press, Ithaca, NY, pp 409–425 McKnight T (1976) Friendly vermin: a survey of feral livestock in Australia. Univ Calif Publ Geography 21:1–104 Mesterton-Gibbons M, Dugatkin LA (1995) Toward a theory of dominance hierarchies: effects of assessment, group size, and variation in fighting ability. Behav Ecol 6:416–423 Miller R (1979) Band organisation and stability in red desert feral horses. In: Denniston RH (ed) Symposium on the ecology and behaviour of wild and feral equids. University of Wyoming, Laramie, pp 113–129 Miller R, Denniston RH II (1979) Interband dominance in feral horses. Z Tierpsychol 51:41–47 Miller RM, Lamb R (2005) The revolution in horsemanship and what it means to mankind. The Lyons Press, Guilford, CT Moehlmann PD (ed) (2002) Equids: zebras, asses and horses. Status survey and conservation action plan. IUCN/SSC Equid Specialist Group. IUCN, Gland, Switzerland, 190 pp Moss CJ, Poole JH (1983) Relationships and social structure of African elephants. In: Hinde RA (ed) Primate social relationships: an integrated approach. Blackwell Science, Oxford, pp 315–325 Naguib M, Fichtel C, Todt D (1999) Nightingales respond more strongly to vocal leaders of simulated dyadic interactions. Proc R Soc Lond B 266:537–542 Nicol CJ (2002) Equine learning: progress and suggestions for future research. Appl. Anim Behav Sci 78:193–208 Nishida T (1983) Alpha status and agonistic alliance in wild chimpanzees (Pan troglodytes schweinfurthii). Primates 24:318–336 Oliveira RF, McGregor PK, Latruffe C (1998) Know thine enemy: fighting fish gather information from observing conspecific interactions. Proc R Soc Lond B 265:1045–1049 Parker GA (1984) Evolutionary stable strategies. In: Krebs JR, Davis NB (eds) Behavioural ecology, 2nd edn. Blackwell Scientific Publication, Oxford, pp 30–61 Paz-y Miño GC, Bond AB, Kamil AC, Balda RP (2004) Pinyon jays use transitive inference to predict social dominance. Nature 430:778–781 Pollock JI (1980) Behavioural ecology and body condition change in New Forest ponies. RSPCA Scientific Publications, Horsham, Great Britain Popper KR (1977) Natural selection and the emergence of mind. Dialectica 22 3:339–355 Pusey AE, Packer C (2003) The ecology of relationships. In: Krebs JR, Davis NB (eds) Behavioural ecology, 4th edn. Blackwell Scientific Publications, Oxford, pp 254–283 Reluga TC, Viscido, S (2005) Simulated evolution of selfish herd behavior. J Theor Biol 234:213–225 Rivera E, Benjamin S, Nielsen B, Shelle J, Zanella AJ (2002) Behavioral and physiological responses of horses to initial training: the comparison between pastured versus stalled horses. Appl Anim Behav Sci 78:235–252 Rubenstein DI (1978) Islands and their effect on the social organisation of feral horses. Paper 100, Anim Behav Soc Annual Meeting, Univ Washington, Seattle, June 19–23, 1978 Rubenstein DI (1981) Behavioural ecology of island feral horses. Equine Vet J 13:27–34

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Chapter 10

African Mole-Rats: Eusociality, Relatedness and Ecological Constraints M. Justin O’Riain(* ü ) and Chris G. Faulkes

Abstract Within the family of African mole-rats (Bathyergidae) there is a range of lifestyles from strictly solitary to eusocial. This variation correlates strongly with numerous ecological factors providing evidence in support of an ecological basis for the evolutionary inception and maintenance of sociality in mole-rats. Furthermore, recent studies on the relatedness of individuals both within and between neighboring colonies of social mole-rats suggest that previous arguments that expounded the importance of relatedness to the evolution of sociality were misleading. A close look at arguably the only eusocial mammal known to science, the naked mole-rat, provides a unique opportunity to study the similarities in the selective environment of insects and mammals without the associated phylogenetic noise of a close common ancestry. In addition, striking examples of convergent evolution between naked molerats and eusocial insects provides insight into why there are so few eusocial vertebrates.

10.1

Introduction African Mole-Rats: Ecological and Social Diversity

African mole-rats are subterranean hystricomorph rodents endemic to subSaharan Africa. The family is speciose with many holotypes being named in the late 19th and early 20th century. Reviewing this early literature, Ellerman (1940) listed a total of 62 species in five genera, as follows: Heterocephalus (n = 4); Heliophobius (n=3); Georychus (n=8); Bathyergus (n=3); Cryptomys (n=49). Currently, the taxonomy of mole-rats is in a state of flux whilst synonymies in the nomenclature are fully investigated using modern techniques. However, recent

M. Justin O’Riain Zoology Department, University of Cape Town, Private Bag X3, Rondebosch, 7701, South Africa [email protected]

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molecular phylogenetic (Faulkes et al. 2004; Ingram et al. 2004) and cytogenetic studies (Van Daele et al. 2004) support the high species diversity in Cryptomys, and suggest splitting this clade into two genera, Cryptomys and Coetomys (Ingram et al. 2004) or Cryptomys and Fukomys (Kock et al. 2006). In this chapter, we will adopt the traditional nomenclature of a single genus (Cryptomys). Figure 10.1 presents a simplified phylogeny showing the relationships between genera, their estimated divergence times and social structure. Mole-rats in the genera Heliophobius, Bathyergus and Georychus all adopt a strictly solitary lifestyle and are generally restricted to regions of higher precipitation (greater than 400 mm per annum). Of these, Heliophobius has the widest distributional range and occurs in the sandy soils of savannas and woodlands of southern Kenya, throughout Tanzania and parts of southeastern Zaire, through Malawi to central Mozambique. The other two solitary genera are much more restricted in their ranges. Bathyergus is endemic to some coastal areas of South Africa and southern Namibia, and Georychus occurs in several disjunct populations within South Africa. In the two remaining genera (Cryptomys and Heterocephalus) all taxa investigated so far exhibit social behavior, and are found in both mesic and xeric regions. Heterocephalus occurs in the arid regions of East Africa (parts of Kenya, Ethiopia and Somalia). The areas they inhabit are characterized by low (less than 400 mm per annum) and unpredictable rainfall, with on average only 4 months per year having more than 25 mm of rain (approximately the quantity required to soften the soil at the depth of foraging tunnels and thus facilitate burrowing; Jarvis et al. 1994). The Cryptomys genus is the most widely distributed of all the extant bathyergids, ranging throughout South Africa, and extending into part of Mozambique and Zimbabwe, and southern, central and western Africa. They are apparently absent from the horn of Africa, tropical rainforests of central and west Africa, and the Sahara. As with Heterocephalus, the ranges of some of these social Cryptomids extend into areas of very low, sporadic and unpredictable rainfall (sometimes <200 mm per annum). However, some species also occur in mesic areas, like the common mole-rat, Cryptomys hottentotus hottentotus. The relationship between sociality and habitat aridity will be discussed in more detail below. Molecular phylogenies of the Bathyergidae are firmly rooted in East Africa, with Heterocephalus and Heliophobius forming the basal lineages (Fig. 10.1), and the common ancestor of the family dated to approximately 40–48 million years ago (Huchon and Douzery 2001). The subsequent adaptive radiation and spread of the family across sub-Saharan Africa appears to have been influenced by Rift Valley formation and its affect on geomorphology, vegetation and climate (Faulkes et al. 2004; Faulkes and Bennett 2007) and the changing patterns of drainage of major river systems (Van Daele et al. 2004; Van Daele et al., 2007). The variation in patterns of social behaviour across the family has presumably been a response to these environmental challenges, and has led to the convergent gains and/or losses of sociality that we will elaborate on below (Fig. 10.1).

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Fig. 10.1 Evolutionary relationships and social strategies in selected species of African mole-rats. Phylogram based on maximum parsimony analysis of 18 bathyergid mtDNA haplotypes (combined 12S rRNA and cytochrome b gene sequences) and outgroup species Thryonomys swinderianus (cane rat). Numbers above each branch refer to the percent bootstrap values following 100 replications after weighting sites with the rescaled consistency index. Estimated divergence times of selected internal nodes are in million years before present (myr; data adapted from Faulkes et al. 1997a, 2004)

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Evolutionary Routes to Sociality

It is generally agreed that the subsocial route, in which offspring delay dispersal and remain with their parents, is the evolutionary origin of most temporally stable mammalian groups. The basic unit is thus the family, which is defined by Emlen (1995, 1997) as: a group where offspring continue to interact with their parents into adulthood, that is, beyond the age of sexual maturity. Emlen (1995, 1997) further differentiates families into simple or extended. In the latter, two or more group members, of either one or both sexes, breed. In simple families, only one pair breeds. In many social mammals, newly founded groups are typically simple families but with time the immigration of unrelated foreign conspecifics results in the family becoming extended. The wide range of lifestyles within a single phylogenetic family has encouraged comparative studies of African mole-rats in an attempt to discern the ultimate factors leading to the evolution of sociality in mammals and the proximate mechanisms that maintain it. In the remainder of this chapter we review our current understanding of these selective factors with the explicit objective of comparing the relative importance of intrinsic genetic versus extrinsic ecological variables in the evolution of cooperative breeding/eusociality in African mole-rats.

10.3

Eusociality: Definitions and Extent

Eusociality is a special form of sociality that has interested biologists since Darwin first considered the existence of sterile castes as a special difficulty for the theory of natural selection. The term ‘eusocial’ was originally used to describe groups of insects living in close-knit communities but where there is a reproductive division of labor. In such social systems, only a small number of individuals are actually involved in direct reproduction. The remainder of the social group is composed of functionally, or irreversibly sterile, non-breeding helpers that cooperate in the rearing of further offspring. In eusocial invertebrates, this functional specialization is often associated with morphological differentiation (i.e., physical castes) between breeders and non-breeders and amongst non-breeders (Michener 1969; Wilson 1971). Since Jarvis’ (1981) discovery of the first eusocial mammal, the naked molerat, it has become increasingly apparent that eusociality, as originally defined, is far more widespread than previously assumed and occurs in many other mammals too. Meerkats (Suricata suricatta), dwarf mongoose (Helogale parvula), wild dogs (Lycaon pictus) and silver backed jackals (Canis mesomelas) are all examples of mammalian species characterized by a reproductive division of labor, an overlap of generations and the co-operative care of offspring born to the group, thus satisfying the original criteria of eusociality (Batra 1966; Michener 1969; Wilson 1971). Furthermore, eusociality is no longer considered to be restricted to

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only two members of the bathyergid mole-rat family (Jarvis and Bennett 1993; Jarvis et al. 1994). Recent studies on the common (Spinks 1998) and Zambian mole-rats (Burda 1993) provide convincing evidence that these species also satisfy the original criteria of eusociality. Given the diversity in social organization among animals, it is important that the terminologies, and a generally accepted understanding of exactly what constitutes a eusocial society, are clearly defined. In an attempt to cater for the ever-widening circle of eusocial species in diverse taxa, various authors, e.g., Kukuk (1994), Gadagkar (1994), Sherman et al. (1995), Crespi and Yanega (1995) have argued for the redefining of eusociality. Arguments (reviewed by Costa and Fitzgerald 1996) range from the expanded view of Sherman et al. (1995), which attempts to classify all species with evidence of reproductive skew as eusocial, to the narrow view of Crespi and Yanega (1995) that argue for the restriction of eusociality to species characterized by irreversible behavioral or morphological castes. Rigid, categorical definitions such as those of Michener and Wilson that have been used to describe eusocial species are perhaps less useful for quantitative comparative studies than some kind of continuous measure of the type proposed by Sherman et al. (1995) and Keller and Perrin (1995). Burda et al. (2000) have attempted to extend the proposal of Emlen (1995, 1997), that natal philopatry produces overlapping generations (a condition of the definition of Wilson 1971), and redefined eusociality by introducing the criterion “permanent philopatry” to replace “overlap of generations”. Permanent, is synonymous with invariable and with few exceptions a wholly inappropriate term to describe social traits. There is nothing permanent about groups of either social insects or vertebrates. Colony fission and/or dispersal are true of all social groups, which is to say that philopatry is never permanent for all colony members and the extent of it varies both within and between species. Decisions about staying at home or dispersing are closely related to ephemeral criteria like rainfall, food availability and the proximity of neighboring groups. Furthermore, it is quite clear that different species may have similar degrees of philopatry but for different reasons and similarly different groups within one species may vary considerably with respect to philopatry, both within and between years. Thus we would argue that by redefining eusociality to include a variable implicit in the formation of all social groups does little more than to add a perfunctory weapon to a long-standing semantic battle. We will only progress in this endeavor if we are successful in correctly identifying biologically real discontinuities (e.g., behavioral castes, Crespi and Yanega 1995; or morphological castes, Beekman et al. 2006) or a common axis to unite all social species under a single theoretical umbrella (e.g., reproductive skew, Sherman et al. 1995). Although both of these approaches have their own problems (Costa and Fitzgerald 1996), it is only by such approaches that the student of sociobiology will gain insight into the evolutionary relevance of the evolved traits. Irrespective of where, or even if, the line between eusociality and other forms of sociality is eventually drawn, all of the above authors concur that the evolutionary origins of eusociality should no longer be considered to lie in intrinsic or

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genetic (e.g., haplodiploidy) factors, given the broad taxonomic range of its occurrence. In essence, we agree with Sherman et al. (1995) that evolutionary explanations for sociality in vertebrates and invertebrates will be best understood if common selective factors are identified rather than independent explanations sought for each taxonomic group. We do not see the heuristic value of the approach taken by Burda et al. (2000) who suggested that sociality is an ancestral trait in African Bathyergid mole-rats and therefore that the appropriate question about the evolution of eusociality in mole-rats should be: Why did certain species of the bathyergid family become solitary and why have Cryptomys and Heterocephalus not abandoned the social way of life? While this approach might be of interest from a point of view of phylogeny it has little or no effect on the hypotheses that address convergence of lifestyles within the family. The real challenge lies in explaining why extant members of the Bathyergid family are both social and solitary irrespective of the lifestyle of their ancestors. If concrete evidence emerged to show that the ancestors of the Bathyergidae were indeed social, then we would ask “what factors promoted sociality in the ancestor?”. What is of special interest in eusocial species is that a large proportion of the adult members of a population do not reproduce. This was one of Darwin’s original special difficulties in his theory of evolution by survival of the fittest. It is for this reason that we have in the past decade, focused our work on the social rather than the solitary species. It does not suffice to state that the reason why these two species are eusocial is simply because that was the ancestral state for members within this species. Rather we should be more concerned with what genetic or ecological factors have promoted or maintained it as a viable way of life, irrespective of whether all species were originally social or solitary. In addition, a number of phylogenies (Allard and Honeycutt 1992; Faulkes et al. 1997a; Walton et al. 2000) show that naked mole-rats and the Cryptomys genus are separated by a number of common ancestors leading to lineages of solitary species, indicating repeated losses and gains of varying degrees of social elaboration. Comparative analysis of the kind carried out by Faulkes et al. (1997a), and criticized by Burda et al. (2000), make independent contrasts with no a priori assumption of the character state of the common ancestor. There is no a priori reason to suppose the ancestor was solitary, as the social traits of a common ancestor could equally have been lost, this so-called secondary solitary has been reported in some species of bees (Wcislo and Danforth 1997). It is generally accepted that when dispersal is constrained, offspring will stay within their natal territory and maximize their fitness by helping their parents to rear other closely related offspring, provided the former benefit from such help. Burda et al. (2000) claim that the question about eusociality is not why the offspring help and do not reproduce but instead why they do not disperse in order to reproduce. We disagree. The essential questions pertaining to eusociality, first posed by Darwin, is why do individuals sacrifice the opportunity to breed and then help others to do so? Limited dispersal might provide the ultimate cue for group formation but it is how individuals living in a group partition reproduction that is the key question about eusociality. Burda et al. (2000) consider the

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proximate mechanism for delayed dispersal as “a behavioral manifestation of attainment of the last stage of puberty”. This statement is refuted by the existence of sexually mature offspring within the natal burrows of Cryptomys mechowi (Bennett et al. 1997) and Cryptomys hotenttotus hotenttotus (Spinks 1998) and the finding that most male naked mole-rat ‘non-breeders’ or helpers do in fact produce sperm. The occurrence of sexually mature adult offspring within a natal group is relatively common amongst mammalian social species, e.g., meerkats (O’Riain et al. 2000), dwarf mongoose (Creel et al. 1992), and wild dog (Creel et al. 1997). Clearly, attainment of the last stage of puberty is not the critical criterion for staying versus leaving decisions in cooperatively breeding mammals. A more parsimonious ultimate mechanism for delayed dispersal is simply that the costs and risks of leaving home are too high and thus individuals are forced to remain at home. When conditions improve, one would expect that only sexually mature adult individuals, capable of reproducing independently, would benefit from leaving. Thus, delayed reproduction is not a cause of delayed dispersal but rather a consequence of it. Socially induced delayed puberty is evident in naked mole-rats (Jarvis et al. 1994) and is a mechanism to maintain high reproductive skew within colonies that will naturally inbreed.

10.4

Genetic Structure of Mole-Rat Colonies

Much of our current data concerning the Bathyergidae emanate from laboratory experiments and observations of captive reared animals. This type of data is particularly weak at estimating pup recruitment (food is supplied ad libitum), natural attrition (no predators) and dispersal rates (animals are confined). Consequently, laboratory estimates of reproductive skew and relatedness of group members, the number of overlapping generations, and the costs and benefits of cooperation are potentially meaningless. Fortunately, both long-term ecological and genetic studies have been completed on wild populations of three social species of mole-rats, the Naked (Brett 1991; Reeve et al. 1990; Faulkes et al. 1997b; Braude 2000), Damaraland (Jarvis and Bennett 1993; Burland et al. 2002, 2004) and Common mole-rats (Spinks et al. 1998, 2000; Bishop et al. 2004) and much support in favor of the laboratory results have emerged. In particular, these studies have confirmed the laboratory observations that new colonies readily form by parental retention of offspring and consequently the genetic structure of groups resembles that of close family members. Furthermore, observations of close inbreeding in laboratory reared colonies of naked mole-rats are supported by results from wild colonies with intra-colony relatedness estimates as high as r=0.8 (Reeve et al. 1990). By contrast, all other social species of mole-rats are obligate outbreeders and laboratory colonies of Cryptomys species will cease reproducing if unrelated animals are not introduced following the death of one of the original breeding pair. Recent work by Burland et al. (2002) and Bishop et al. (2004) uphold these trends and suggest that colonies are largely comprised of close

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family members (i.e., parents and their offspring) but that unrelated individuals are often present and consequently average levels of relatedness are slightly less than expected for a group comprised only of first-order relatives. The exceptionally high relatedness coefficients amongst colony members in naked mole-rat have often been argued to be an important selective factor in the evolution of their eusociality (Reeve et al. 1990; Reeve 1992; Burda 1995; Lacey and Sherman 1997). Higher levels of relatedness offset the costs of helping behavior and thus favors the evolution of group living (and helping) through kin selection (Hamilton 1964). However, helping behavior is equally apparent in social species characterized by lower levels of within colony relatedness. Furthermore a recent study by Hess (2004) suggested that previous studies (e.g., Reeve et al. 1990) greatly overestimated relatedness within and between colonies of naked mole-rats because they failed to take into account environmental and historical influences that could bias the estimate. Hess (2004) reported relatedness values that were not significantly different to the 0.5 level of relatedness expected for siblings from randomly mated parents, although values ranged with geographic scale and sample size. Furthermore Hess’s (2004) analysis of F-statistics indicated this species has an avoidance of inbreeding system of mating, which contradicts previous notions of a routinely inbreeding system. Average levels of relatedness within naked mole-rats may thus be similar to the obligatory outbreeding Damaraland mole-rat. Occasional high levels of relatedness in naked mole-rats are thus likely to be a consequence of greatly limited dispersal opportunities and the subsequent mating of close relatives. Such inbreeding events are themselves a by-product of philopatry amongst related individuals, i.e., group living had to have preceded inbreeding. Thus similar to haplodiploidy in hymenopterans, high levels of relatedness in naked mole-rats are not a prerequisite for the evolution of groups and helping behavior but rather a factor that may contribute to the maintenance of sociality in these species (see also Chaps. 3, 5, 6, 7). Relatedness also fails to explain certain behaviors observed within captive naked mole-rat colonies, particularly those pertaining to dominance and reproductive conflict. Queens direct their aggression predominantly towards larger, older colony members irrespective of their relatedness (Jacobs and Jarvis 1996). Following the death of a queen there is often lethal fighting amongst females to take over her position as the sole breeding female. Fighting is particularly fierce amongst the larger, older females within the colony and, similar to queen aggression, does not correlate inversely with relatedness. Indeed individuals that are more similar in age and therefore body mass (O’Riain and Jarvis 1998) are typically full siblings. One particular example from a captive colony of naked mole-rats at the University of Cape Town serves to highlight the failure of relatedness to explain patterns of aggression within colonies. A colony comprised of a founding breeding pair and their first four successive litters suffered the loss of its’ breeding male. A new male was introduced 5 months later and after a year he successfully sired and helped to raise four subsequent litters with the original queen. The colony was thus comprised of two lots of four litters that were each full siblings but the relatedness between the groups was that of half siblings.

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Following the death of the original queen, severe fighting broke out and a new queen emerged from the older group of full siblings. The new queen then systematically killed all of her full-siblings over a period of 11 months until the colony was comprised only of her and her younger half-siblings who then helped her to raise her offspring. This preferential killing of closer relatives is contrary to predictions based purely on levels of relatedness within kinselection theory. The most parsimonious explanation for this unusual behavior is that the queen maximized her direct fitness benefits by killing all those individuals that were closely matched to her in terms of size, i.e., her closest competitors. Maximizing direct fitness benefits may also provide a better explanation than indirect for rates of food provisioning in naked mole-rats. O’Riain (1996) showed that rates of food provisioning to the communal nest did not correlate with the level of relatedness of helpers to either the queen or her most recent litter. Rather, the helping behavior of food provisioning was subject to the selfish precedent of satiation. Similar results were obtained by Clutton-Brock et al. (1998) for guarding behavior in meerkats. Individuals were significantly more likely to engage in the guarding if they were satiated and there was no significant effect of guarding contributions and the mean levels of relatedness to other colony members. It seems obvious that high levels of relatedness in mammalian social groups are largely a consequence of groups forming through natal philopatry. While it is not possible to discount the possible contributing effects of kin-selection to the evolution of helping behavior and sociality within these societies, it is equally impossible to explain many of the individual level behaviors using inclusive fitness theory. By contrast, direct fitness benefits readily explain the lack of kin bias within social mammal species (see also Griffin and West 2003) but don’t explain why groups of kin formed in the first instance. If relatedness alone does not suffice to explain the formation of groups of closely related individuals then the question thus arises as to what ecological constraints have driven the evolution of sociality in this family of African rodents?

10.5

Ecological Constraints: Aridity and Food Distribution

A number of authors have proposed that the distribution, size and digestibility of the geophytes upon which mole-rats feed, as well as the variation and predictability of rainfall have played a pivotal role in the evolution of sociality in the Bathyergidae (Jarvis 1978; Bennett 1988; Lovegrove and Wissel 1988; Lovegrove 1991; Jarvis et al. 1994; Faulkes et al. 1997a; Jarvis et al. 1998). This has become known as the “aridity-food-distribution hypothesis” (AFDH). Sexually mature adults that retain their offspring would benefit from increased survival of their offspring in addition to increased personal survival. Parents that evicted their offspring were unlikely to be able to successfully procure sufficient food and their offspring would suffer similar problems. The net result would be a loss in fitness of the parents and the

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lifetime reproductive success of the offspring. Thus the evolutionary inception of sociality is argued to be parental retention of offspring in the natal territory and the question thus becomes: what factors promote sociality as a successful lifestyle, given the obvious direct fitness benefits? Burda et al. (2000) state, that the AFDH may provide an explanation for why cooperative foraging is necessary for survival in an arid habitat. Following on directly from this we suggest that deriving the criteria of eusociality thereafter is relatively simple: (1) parents maintain a monopoly on reproduction because of incest avoidance (2) there is an overlap of generations because of the high costs and risks associated with offspring dispersal and independent foraging and (3) cooperative care of the young born to the colony is expected because helping to raise related young is the best way for offspring, that cannot breed independently, to increase their inclusive fitness (Hamilton 1964). Burda et al. (2000) insist that if the AFDH were a viable explanation for eusociality of mole-rats then one would expect to see evidence for convergence among unrelated taxa in similar habitats. This is exactly what we do see. Heterocephalus glaber, Cryptomys damarensis and C. h. hottentotus all occur in arid habitats in which foraging is both costly and risky and they have evolved to live in social groups. The latter species, may also be found in more mesic areas, an observation often used to argue against the AFDH. To say that the presence of solitary species (e.g., Bathyergus janetta) living in arid areas provides evidence against the AFDH is to grossly oversimplify the hypothesis. Aridity per se is insufficient as an explanation for group living. The AFDH is a combination of aridity (A) and food distribution (FD). Evidence against the AFDH would need to provide examples of species that are solitary under conditions of unpredictable and limited rainfall in addition to food resources that are patchily distributed and located at considerable energetic costs. B. janetta is often found in association with subterranean moisture seepage areas, and where food resources are abundant in these otherwise very arid regions. The AFDH has never claimed that social species cannot occur in mesic areas, only that sociality evolved in arid regions and that social mole-rats may subsequently migrate into mesic regions. Burda et al. (2000) also expect to see evidence of divergence of social structure among related taxa in different habitats. Spinks et al. (1998, 2000) has shown that within a single species the social structure varied along an aridity gradient, with colonies in more arid regions having a social structure more similar to that of the ‘eusocial’ species, with a greater degree of philopatry, reproductive skew, and overlap in generations suggesting a strong link between the environment and life-history traits. Colony size, a variable frequently associated with the degree of sociality, has not been directly discussed under the predictions of the AFDH (Jarvis et al. 1994; Faulkes et al. 1997a). All social species are philopatric to some degree but none permanently so. The degree of philopatry is affected by the quality of the habitat. It has been shown that in a number of social mammal species e.g., dwarf mongoose (Creel et al. 1992), naked mole-rats (Braude 2000), Damaraland mole-rats (Jarvis and Bennett 1993) and meerkats (Clutton-Brock et al. 1998), and social birds (see Chap. 8) that dispersal is strongly linked to ecological conditions and that dispersal rates are higher when food is more abundant (see Chap. 7, for an alternative dispersal

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scenario in wood termites). Faulkes et al. (1997a) used maximum group size as an indication of sociality and constraints on dispersal. What is apparent from the analysis is that in habitats with higher constraints on dispersal, group sizes are generally greater. The fieldwork carried out Braude (2000) on naked mole-rats revealed colonies of 250 and 290 individuals, with approximately 20% of the 54 colonies sampled numbering over 120 individuals. While colony sizes in excess of 60 have been reported for C. mechowi, by Burda and Kawalika (1993) this data was obtained by interviewing local hunters and then classifying the replies as irrational, pseudo-rational, or rational. Only “rational” replies were accepted as fact, and using this somewhat unscientific approach, colony size estimates obtained. In the absence of more rigorous data these estimates of colony size have been largely disregarded and the largest colony sizes, second to naked mole-rats, are those recorded by Jarvis and Bennett (1993) of 41 for C. damarensis. When the costs of dispersal are constantly high then offspring will benefit from staying at home until ecological conditions improve and the benefit to cost ratio is favorable for dispersal. Thus it follows logically that conditions that allow for reproduction but limit dispersal will result in a trend towards larger group size provided all other variables (e.g., predation) are fairly constant. A further variable influencing group size is the longevity of breeders. Naked mole-rats are the longest lived small mammals in the world with females capable of sustained reproduction for 27 years (unpublished data). The breeders are thus capable of producing large numbers of offspring for a sustained period which when coupled with low dispersal rates and facultative inbreeding is thought to account for the largest known group sizes (up to 300 individuals) for a cooperatively breeding mammal. By contrast, dispersal rates in other social bathyergids are high, breeder survival is low and most species studied to date are obligate outbreeders. Thus the maximum colony size attained by the ‘haired’ social mole-rats is 40. This raises the question about the limits to mammalian sociality and whether inbreeding might explain why extreme reproductive lifespan and facultative inbreeding in naked mole-rats are the key variables that make them an exception to other social vertebrates.

10.6

Naked Mole-Rats—the Only Eusocial Mammal?

Superficially, it is easy to understand why for over a decade, naked mole-rats were regarded as the world’s only eusocial mammal. Their large colony size and Jarvis’ (1981) reference to morphological and behavioral worker castes within colonies provided a strikingly close parallel to eusocial insect colonies. However, neither colony size nor the presence of castes, are prerequisites of the original definition(s) of eusociality (Michener 1969; Wilson 1971). Curiously, there were published studies on other mammals (e.g., Rasa 1977; Frame et al. 1979; Moehlman 1979) that had already satisfied the three original criteria of eusociality viz. a reproductive division of labor, an overlap of generations and the cooperative care of young, but none of these authors had capitalized on the important scientific link

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with eusocial insects. The unique status of naked mole-rats has been gradually eroded by the realization that many social mammals do indeed satisfy the original definition of eusociality. Subsequent redefining of eusociality either included all social mammals on a continuum of reproductive skew (Sherman et al. 1995) or excluded all social vertebrates because their young are totipotent (the potential throughout life to exhibit the full behavioral repertoire of the species) (Crespi and Yanega 1995). Both definitions served to further strip naked mole-rats of their previously unique social status amongst vertebrates. However, with the discovery by O’Riain et al. (2000) that female naked molerats undergo a physical transformation following the attainment of reproductive status (similar to physogastry in eusocial termites), the debate concerning the uniqueness of this species amongst vertebrates has resurfaced. O’Riain et al. (2000) presented convincing data that complete dimorphism exists within colonies and that these physical differences equate to irreversible morphological castes sensu queens and workers of eusocial termite queens. Previous use of the term caste with reference to mole-rats was erroneous (e.g., Jarvis 1981; Bennett 1988) for the differences amongst workers were not discrete but rather based on continuous variables such as body mass and work rate. The finding that a mammal has evolved morphologically discrete queen/worker castes is the most convincing evidence to date of convergent evolution in the lifestyle of an insect and mammal and it begs the question as to what the common selective factors are? Both termites and naked mole-rats live within a secure fortress, which affords the reproductives a high degree of safety from predation (see Chap. 7). However, the same is true for all other mole-rat species that do not have physical castes and many insect species without queens, so this alone is insufficient as an explanation. A characteristic shared by naked mole-rats and many lower termite species is that of facultative inbreeding (Bartz 1979; Reeve et al. 1990; Faulkes et al. 1997b; O’Riain and Braude 2000; Chap. 7). In addition, both groups have evolved specialized dispersal morphs for occasional outbreeding (Bartz 1979; Noirot and Pasteels 1987; Roisin 2000; O’Riain et al. 1996) when ecological conditions are optimal (e.g., after good rainfall). Obligatory outbreeding mole-rats in addition to eusocial insect species like honeybees require foreign conspecifics to ensure continued reproduction within the colony. Following the death of a breeding male, such molerat colonies typically fragment (Jarvis and Bennett 1993) and breeding females are forced to disperse, forage and defend their new burrow systems. A similar pattern has been observed in many cooperative breeding birds (Emlen 1997), which effectively prevents the formation of large groups—‘higher’ sociality. Similarly, honeybee queens are forced to embark on further nuptial flights once their spermathecae are empty. It is obvious that the selective potential for becoming morphologically specialized (e.g., physogastric) is greatly reduced for females who are not free to specialize exclusively on reproduction but who rather are subject to selection for subsequent dispersal and only then further reproduction. Both termite and naked mole-rat queens by contrast are long-lived and exempt from dispersal once established within their colonies as they can readily inbreed. Furthermore, they do not have to engage in either costly or risky

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behaviors (e.g., foraging and colony defense) and are free to focus their time and energies on reproduction. It is perhaps not surprising therefore that queens in both higher termites and naked mole-rats outlive helpers by orders of magnitude (Sherman and Jarvis 2002), while such differences are negligible in most other social animals. Differences in longevity between helpers and breeders, together with much larger colonies, have dramatic consequences for the probability that a given helper can fill a breeding vacancy and hence greatly affects lifetime variation in reproduction. Such divergence in selection pressures within a colony affects the scope of natural selection on individuals (Bourke 1999). Morphologically specialized breeders that are not required to perform the helper role will be selected for increased fecundity. Conversely, when helpers lose the option to breed, natural selection will favor those individuals best adapted to increase their inclusive fitness via non-reproductive activities. Thus natural selection can favor breeding-female naked mole-rats that specialize more extremely in reproduction through permanent morphological changes. With an increase in colony size, because of the ecological constraints on dispersal, the probability that a particular non-breeding female would fill any within group reproductive vacancy in its lifetime decreases. Thus the evolutionary stage was set for individuals to follow one of two different life-history trajectories, worker or breeder, and ultimately for the evolution of completely dimorphic morphological castes. When helpers are behaviorally but not morphologically specialized, i.e., they still have the possibility to reproduce later in life, selection will not favor adaptations aimed solely at increasing inclusive fitness via helping (sensu lower termites, see Chap. 7). Hence, no vertebrate studied to date has been shown to have evolved castes amongst the non-breeders and all specializations observed are behavioral, e.g., defense and work-related activities (O’Riain and Jarvis 1997). Termite, ant, and naked mole-rat queens with their enlarged abdomens and long life-spans provide a striking example of convergent evolution in response to ecological selection pressures.

10.7

Concluding Comments

Ultimate evolutionary factors that have been recognized as important to the evolution of sociality in mammals are (1) predator vigilance and protection, e.g., meerkats (Clutton-Brock et al. 1998), dwarf mongoose (Rasa 1977), naked mole-rats (Alexander et al. 1991); and (2) increased efficiency in procuring food, e.g., naked mole-rats (Jarvis 1985), Damaraland mole-rats (Jarvis and Bennett 1993), wild dog (Frame et al. 1979) and wolves (Zimen 1975). Burda et al. (2000) suggest that the ultimate evolutionary reason for eusociality in mole-rats is that it is a phylogenetically constrained phenomenon resulting from a social common ancestor of the Bathyergidae. Eusociality may well be the ancestral state of all mole-rats and this is without a doubt an interesting and valid point to consider, but this approach merely side-steps the issue of what selective factors ultimately may have given rise to natal

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philopatry and cooperation in ancestral bathyergid species in the first place. The mere fact that there are both solitary and social species of mole-rats in the same family means that factors other than the social status of the common ancestor must be evoked to explain the different life-styles. Cooperative breeding/eusociality is a social system present in a diverse array of species, from coral reef shrimps (Duffy 1996) to wild dogs (Creel et al. 1997). Such dramatic examples of convergent evolution in taxonomically disjunct groups demonstrate the futility of arguments that attempt to explain the evolution of philopatry and cooperative breeding by referring to the ancestry of a given species. Common selective factors must be sought to explain a common lifestyle, not only amongst mole-rats in the same family but also in the many different taxa that evolved a lifestyle characterized by philopatry and reproductive skew. In this chapter we consider the respective influence of relatedness and ecological constraints on the evolution of sociality in African mole-rats. We conclude that it is not possible to rule out the influence of kin-selection because all vertebrate social groups are formed through natal philopatry (i.e., the subsocial evolutionary route). However, relatedness alone is inadequate to explain the variation in sociality evident both within the family and within species. Ecological constraints emerge as the most significant selective factor for group formation and ultimately, the evolution of castes in the most social of all mammals—the naked mole-rat.

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Ingram CM, Burda H, Honeycutt RL (2004) Molecular phylogenetics and taxonomy of the African mole-rats, genus Cryptomys and the new genus Coetomys gray, 1864. Mol Phyl Evol 31:997–1014 Jacobs DS, Jarvis JUM (1996) No evidence for the work conflict hypothesis in the eusocial naked mole-rat (Heterocephalus glaber) Behav Ecol 39:401–409 Jarvis JUM (1978) Energetics of survival in Heterocephalus glaber (Ruppell), the naked mole-rat (Rodentia: Bathyergidae). Bull Carnegie Mus Nat Hist 6:81–87 Jarvis JUM (1981) Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212:571–573 Jarvis JUM (1985) Ecological studies of Heterocephalus glaber, the naked mole-rat, in Kenya. Natl Geogr Soc Res Rep 20:429–437 Jarvis JUM (1991) Reproduction in naked mole-rats. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp 384–425 Jarvis JUM, Bennett NC (1993) Eusociality has evolved independently in two genera of bathyergid mole-rats, but occurs in no other subterranean mammal. Behav Ecol Sociobiol 33:353–360 Jarvis JUM, O’Riain MJ, Bennett NC, Sherman PW (1994) Mammalian eusociality: a family affair. Trends Ecol Evol 9:47–51 Jarvis JUM, Bennett NC, Spinks AC (1998) Food availability and foraging by wild colonies of Damaraland mole-rats (Cryptomys damarensis): implications for sociality. Oecologia 113:290–298 Keller L, Perrin N (1995) Quantifying the level of eusociality. Proc R Soc Lond B 260:311–315 Kock D, Ingram CM, Frabotta LJ, Honeycutt RL, Burda H (2006) On the nomenclature of Bathyergidae and Fukomys N. Gen. (Mammalia: Rodentia). Zootaxa 1142:51–55 Kukuk PF (1994) Replacing the terms “primitive” and “advanced” New modifiers for the term “eusocial”. Anim Behav 47:1475–1478 Lacey EA, Sherman PW (1997) Cooperative breeding in naked mole-rats: implications for vertebrate and invertebrate sociality In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, New York, pp 267–301 Lovegrove BG, Wissel C (1988) Sociality in mole-rats: metabolic scaling and the role of risk sensitivity. Oecologia 74:600–606 Lovegrove BG (1991) The evolution of eusociality in mole-rats (Bathyergidae): a question of risks, numbers and costs. Behav Ecol Sociobiol 28:37–45 Michener CD (1969) Comparative social behaviour of bees. Annu Rev Entomol 14:299–342 Moehlman PD (1979) Jackal helpers and pup survival. Nature 277:382–383 Noirot C, Pasteels J (1987) Ontogenetic development and evolution of the worker caste in termites. Experientia 43:851–860 O’Riain MJ (1996) Pup ontogeny and factors influencing behavioural and morphological variation in naked mole-rats, Heterocephalus glaber (Rodentia, Bathyergidae) O’Riain MJ, Jarvis JUM, Faulkes CG (1996) A dispersive morph in the naked mole-rat. Nature 380:619–621 O’Riain MJ, Jarvis JUM (1997) Colony member recognition and xenophobia in the naked mole-rat (Heterocephalus glaber). Anim Behav 53:487–498 O’Riain MJ, Jarvis JUM (1998) The dynamics of growth in naked mole-rat colonies - the effects of litter order and changes in Social structure. J Zool Lond 246:49–60 O’Riain MJ, Braude SD (2000) Inbreeding and outbreeding in naked mole-rats. In: Evolution of Dispersal. In: Danchin E, Clobert J, Stenseth N (eds), pp 143–154. Oxford University Press O’Riain MJ, Jarvis JUM, Buffenstein R, Alexander R, Peeters C (2000) Morphological castes in a vertebrate. Proc Natl Acad Sci USA 97:13194–13197 Rasa OAE (1977) The ethology and Socio-biology of the Dwarf mongoose (Helogale undulate parvula). Z Tierpsychol., 43:337–406 Reeve HK, Westneat DF, Noon WA, Sherman PW, Aquadro CF (1990) DNA ‘fingerprinting’ reveals high levels of inbreeding in colonies of the eusocial naked mole-rat. Proceedings of the National Academy of Science of the USA 87:2496–2500

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Reeve HK (1992) Queen activation of lazy workers in colonies of the eusocial naked mole-rat. Nature 358:147–149 Roisin Y (2000) Diversity and evolution of caste patterns. In: T. Abe, D.E. Bignell and M. Higashi, Editors, Termites: Evolution, Sociality, Symbioses, Ecology, Kluwer, Netherlands, pp 95–119 Sherman PW, Lacey EA, Reeve HK, Keller L (1995) The eusociality continuum. Behav Ecol 6:102–108 Sherman PW, Jarvis JUM (2002) Extraordinary life spans of naked mole-rats (Heterocephalus glaber), J Zool Lond 258:307–311 Spinks AC (1998) Sociality in the common mole-rat. Cryptomys hottentotus hottentotus, Lesson 1826: the effects of aridity. Unpubl PhD Thesis, University of Cape Town, South Africa Spinks AC, O’Riain MJ, Polakow DA (1998) Intercolonial encounters and xenophobia in the common mole-rat, of the common mole-rat, Cryptomys hottentotus hottentotus (Bathyergidae): the effects of aridity, sex and reproductive status. Behav Ecol 9:354–359 Spinks AC, Jarvis JUM, Bennett NC (2000) Differential patterns of philopatry and dispersal in an arid and a mesic population of the common mole-rat, and their implications for the evolution of sociality in the African mole-rats. J Anim Ecol 69:224–234 Van Daele PAAG, Faulkes CG, Verheyen, E, Adrianes D (2007) African mole-rats (Bathyergidae): a complex radiation in Afrotropical soils. In: Begall S, Burda H, Schleich CE (eds) Subterranean rodents: news from underground. Springer, Berlin Heidelberg New York, pp 357–373 Van Daele PAAG, Dammann P, Kawalika M, Meier J-L, Van De Woestijne C, Burda H (2004) Chromosomal diversity in Cryptomys mole-rats (Rodentia: Bathyergidae) in Zambia; with the description of new karyotypes. J Zool Lond 264:317–326 Walton AH, Nedbal MA, Honeycutt RL (2000) Evidence from Intron 1 of the nuclear tranthyretin (Prealbumin) gene for the phylogeny of African mole-rats (Bathyergidae). Mol Phylo Evol 16(3):467–474 Wilson EO (1971) The insect societies. Harvard University Press, Cambridge Wcislo WT, Danforth BN (1997) Secondarily solitary: the evolutionary loss of social behavior. Trends Ecol Evol 12:468–474 Zimen E (1975) Social dynamics of the wolf pack. In: Fox MW (Ed) The Wild Canids: Their Systematics, Behavioural Ecology and Evolution. Van Norstrand Rheinhold, New York, pp 336–362

Chapter 11

Genetic and Ecological Determinants of Primate Social Systems Peter M. Kappeler

Abstract Kin-selection theory provides an evolutionary framework for the analysis of the effects of genetic relatedness on animal social systems. The aim of this chapter is to review postulated causal relationships between kinship patterns and social systems in non-human primates. In this context it is crucial to distinguish between social organization, i.e., the size and composition of a social unit, and its social structure, i.e., the pattern of social interactions among the members of a social unit. Current theories about the determinants of primate social systems yield predictions about where and why relatives should live together. Results of the available studies of the genetic structure of primate societies indicate deviations in several cases from expected patterns, however. The socioecological model, which has been widely used to analyze and explain relationships among ecological, social and genetic factors, on the one hand, and social structure, on the other hand, has therefore presumably overestimated the effects of kinship on primate social systems.

11.1

Introduction

Kinship and social behavior are closely intertwined. On the one hand, the degree of relatedness between a pair of individuals determines many aspects of their social behavior, e.g., whether they are likely to cooperate or to mate with each other. One the other hand, aspects of social systems have a profound impact on the genetic structure of animal societies, and, thus, the distribution of kin in space and time. The modulation of cooperative, sexual and competitive behavior, in particular, by the degree of genetic similarity continues to be analyzed with the aid of kin-selection theory (Hamilton 1964). The evolution of a whole range of phenomena, ranging from cooperation among bacteria (Brown and Johnstone 2001) and altruism in amoeba (Strassman et al.

Peter M. Kappeler Dept. Sociobiology/Anthropology, University of Göttingen & Dept. Behavioural Ecology & Sociobiology, German Primate Center, Göttingen, Germany [email protected]

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2000) to infanticide in primates (van Schaik 2000a), has been explained within this theoretical framework. However, previous studies of kin selection have also been plagued by a number of shortcomings. For example, kin relations had to be largely inferred from demographic data in some taxa and relatedness through the paternal line remained unknown. Moreover, the costs and benefits of a particular altruistic act, the modulating effects of ecological variables or social factors other than kinship, the social competence of partners, the role of reciprocity, or the fact that kin also compete with each other, have been ignored in some previous studies, so that a reappraisal of the effects of kinship on social behavior seems warranted (see Chap. 12). Primates, with their diversity of social systems and complex social behavior, provide a rich opportunity to examine interactions between kinship and social systems against the background of a mammalian body plan and life history. In order to contribute comparative information on the ecology of social life, this chapter has the following specific aims: (1) to briefly summarize relevant assumptions and predictions of kin-selection theory, (2) to illustrate the relevant diversity of primate social systems, (3) to examine the determinants of different genetic structures, (4) to review the available data on the genetic structure of primate societies, and (5) to examine the consequences of different genetic structures for primate social behavior in light of the socioecological model that integrates these effects into a single explanatory framework. For more detailed reviews of particular taxa and of alternative behavioral or evolutionary mechanisms, the interested reader is referred to several recent reviews of kin selection and cooperation in primates and humans (Silk 2002a; contributions to Kappeler and van Schaik 2006).

11.2

Kin Selection

Kin-selection theory provides a theoretical framework for the analysis of different pro-social behaviors, such as altruism and cooperation, but also for other aspects of social behavior, such as competition and selfishness (Hamilton 1963, 1964). Kin selection is an evolutionary mechanism that promotes the spread of alleles that are identical by descent through kin. Together with the direct fitness component derived from individual reproduction, such indirect fitness gains define the inclusive fitness of an individual. Kin selection can therefore explain altruistic acts and traits that compromise individual survival and reproduction if they enhance the fitness of relatives. Such phenotypic altruism has originally been explained though group selection (Darwin 1871; Wynne-Edwards 1962), which, however, is clearly not an evolutionary stable strategy (Maynard Smith 1964). More recent alternative group selection approaches focusing on trait group or multilevel selection (e.g., Wilson and Dugatkin 1997) have a much more limited and largely hypothetical applicability than kin-selection theory, which continues to provide the principal explanation of helping and other forms of altruism (Foster et al. 2006). Hamilton’s (1964) inequality can be used to predict whether an altruistic behavior will be able to spread in a population or not. It weighs the benefits of a

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behavior pattern by the coefficient of relatedness between two actors and compares them to the attendant costs. Accordingly, altruistic behavior will evolve most easily whenever the costs are relatively small, the benefits are relatively great and the coefficient of relationship is high. It is therefore assumed that patterns of cooperation and competition among close kin have been shaped importantly by kin selection (Clutton-Brock 2002; Emlen 1994; Johnstone and Dugatkin 2000). However, several caveats and additional factors have sometimes been ignored. For example, indirect benefits accrued through kin selection need to be discounted by the local costs of unavoidable competition among relatives, which is also rife in nature (West et al. 2001; 2002). Reproductive skew, which is theoretically affected by the degree of relatedness among competing individuals (Johnstone 2000), provides one of the best-studied examples of this effect. Furthermore, some cases of altruistic behavior may in fact represent situations in which the actor benefits directly, so that mutualism or selfishness provide more appropriate explanations than kin selection (Clutton-Brock 2002; 2006). Moreover, reciprocity may be a more widespread proximate mechanism facilitating cooperation than previously thought (Trivers 2006; De Waal and Brosnan 2006; Mitani 2006), and other mechanisms of social transactions, such as market effects, provide promising models to explain complex social exchanges without invoking kin selection (Barrett and Henzi 2006; Noe 2006). Finally, kin biases in behavior may in some cases be simply the result of enhanced familiarity or association (Chapais 2001) and kin may not always be the most competent partners for a particular interaction (Chapais 2006). Because most of these points, as they relate to primates, have been examined in a recent collection of essays (Kappeler and van Schaik 2006), the present contribution will focus on yet another aspect—the genetic structure of primate societies and their logical translation into behavioral variation.

11.3

Diversity of Primate Social Systems

Compared to many other mammals, the social behavior of primates is complex and highly diverse. In order to interpret effects of kin selection on primate sociality, we need to determine the genetic structure of primate societies, which in turn also requires information about the mechanisms that modify them. Functional analyses of social systems, not only those of primates, continue to be hampered by a lack of clear definitions and resulting confusion about the targets and mechanisms of selection, however (Kappeler and van Schaik 2002). It is therefore useful to begin such an analysis by reiterating the distinction among different levels and components of social systems. Analyses of social systems deal with the diversity of animal societies observed in nature. A society or social unit can be operationally defined as a set of individuals of the same species that interacts regularly with each other, and more so than with members of other societies. Primatologists distinguish among three aspects of societies that are collectively summarized as the social system (Kappeler and van

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Schaik 2002). First, social organization describes the size, age and sex composition, as well as the cohesion of a society in space and time. Second, social structure describes the patterning of social interactions and the social relationships that emerge from them. Third, the mating system is separated heuristically to summarize sexual interactions. In recent years, behavioral observations of the “who mates with whom?” have been increasingly accompanied by genetic analyses, so that the genetic mating system (“who reproduces with whom?”) can be determined as well. For the present purpose, social organization and social structure are of particular interest because of the presumed direct relationship between them, on the one hand, and kin structure, on the other hand, although mating decisions are also affected by the relatedness between potential mates (see e.g., Pusey and Packer 1987; Starin 2001). Primates, as a relatively small mammalian order, exhibit a stunning diversity of social organizations, which represents the majority of types of organizations found among mammals in general (Davies 1991). This diversity ranges form solitary individuals, through pairs and groups of varying sizes and composition, to stable associations of hundreds of individuals living in hierarchically structured societies. This diversity can be broadly classified into three categories (Kappeler and van Schaik 2002). In solitary species, adults spend the majority of their active phase foraging alone and without immediate coordination of their activities with conspecifics. Some solitary species, however, form small groups during their period of inactivity. It is little appreciated that more than a quarter of the 300 or so primate species are solitary, all of which, with the exception of the orangutan, are relatively small and nocturnal. In pair-living species, one adult male and one adult female are permanently associated and coordinate their activities with each other. This category encompasses about 10% of all primates, which is considerably more than in other mammalian orders (van Schaik and Kappeler 2003). Finally, the majority of primates live in permanently bisexual groups of three or more adults, which distinguishes primates from most other gregarious mammals (van Schaik and Kappeler 1997). The size, sex ratio and cohesion of primate groups are highly variable among species and higher taxa. The evolutionary determinants of this diversity have been studied in detail in recent decades. It is nowadays assumed that individual survival and reproduction are maximized in a particular social organization, given particular combinations and interactions of ecological (resource distribution, predation risk), intrinsic (body size, activity, life history) and social (reproductive strategies, infanticide risk, relatedness) factors (Terborgh and Janson 1986; van Schaik and van Hooff 1983; Wrangham 1980; 1987). Different types of social organization are therefore not the result of selective forces at the level above the individual, but rather the result of many individual decisions that are constantly being evaluated by natural and sexual selection. The relative importance of these factors, as well as phylogenetic constraints on social organization (DiFiore and Rendall 1994; Kappeler 1999a), have been reviewed extensively (Janson 2000; Kappeler 1999b; Nunn and van Schaik 2000), but the questions of where and why relatives live together have received much less attention.

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229

Determinants of Genetic Structure

In all three basic types of social organization, four demographic mechanisms (births, deaths, immigration and emigration) determine the size and composition of a particular society (Cohen 1969). The two mechanisms of migration are of particular interest with respect to the present set of questions because they affect sexually mature individuals, because they are typically sex-specific, and because their expression can become canalized over evolutionary times. As in most mammals (Greenwood 1980; Waser and Jones 1983), males of most primate species emigrate from their natal social unit upon reaching sexual maturity (Pusey and Packer 1987). The few primate species with male philopatry include our closest living relatives, chimpanzees and bonobos. Finally, there are a number of primate species in which both sexes migrate between social units, including most pair-living species and many New World monkeys (Isbell and van Vuren 1996; Moore 1984; Pope 2000). Sex-specific patterns of migration have important genetic consequences because the members of the resident sex develop, over evolutionary times, a higher average degree of relatedness among each other (Bohonak 1999; Ranta et al. 1999; Storz 1999). This process leads to the formation of either matrilines or partilines among the permanent residents of a social unit. As a result of this sex difference in migration patterns and their genetic consequences, sex differences in cooperative and competitive behavior pattern are theoretically expected. A fundamental question in this context is concerned with sex differences in migration. The task consists of identifying and comparing the relative costs and benefits of staying and dispersing, respectively, between the sexes. In the majority of primates, female philopatry, in combination with male emigration, is the rule (Greenwood 1980). Most of female philopatric species have a polygynous mating system, in which male reproductive success is limited by access to estrous females and in which males provide no direct paternal care (Clutton-Brock 1989a). Over evolutionary times, males that have deserted fertilized females in search of additional mates have enjoyed greater reproductive success than others pursuing alternative strategies. Because females cannot expect to obtain paternal care and because their reproductive success is quantitatively unaffected by additional matings (because litter size equals one in most species), their reproductive success is primarily limited by access to resources, whose energy is allocated to supporting pregnancy and lactation. Because foraging efficiency is presumably positively affected by familiarity with an area and the temporal and spatial availability of the resources therein, females may enjoy greater benefits from staying in a familiar area than males. As soon as an initial female advantage in this direction exists, it can be reinforced by the cooperative defense of resources by related females against groups of neighboring females (Pusey and Packer 1987; Wrangham 1980). Even though it would also be advantageous for males to remain and forage in a familiar area, they can encounter more potential mates by roaming over larger areas. This general male tendency to disperse is reinforced by reproductive competition among males that can lead to evictions or voluntary secondary dispersal into

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other social units (Alberts and Altmann 1995; Jack and Fedigan 2004a, 2004b). As soon as a tendency for such a sex difference in dispersal tendencies is established, it will get reinforced by mate choice of resident females through inbreeding avoidance (Clutton-Brock 1989b; Lehmann and Perrin 2003). The modal pattern of female philopatry and male dispersal among primates, as well as the widespread lack of intraspecific variation in these behaviors, can therefore be attributed to the higher relative benefits of staying for females and of dispersing for males, respectively. The costs of emigration are probably similar for both sexes. They include an increased predation risk during migration, reduced foraging success in unfamiliar areas, as well as the risks associated with aggression from the resident competitors of the same sex in the new social unit (Alberts and Altmann 1995). Another question in this context is whether the same factors can also explain the rarer, inverse pattern of male philopatry and female emigration. Most primate species with this dispersal system are still poorly studied, but there are indications that their most important resources are of such a nature that joint resource defense is either not possible or economically unfeasible (Isbell and van Vuren 1996; Moore 1984; Watts 1990). In this case, the benefits of female philopatry would be significantly compromised, so that other, mostly social factors can determine which sex disperses. Such potential social advantages have been identified for both sexes. In some species, such as chimpanzees, there appear to exist highly profitable male reproductive strategies that include the joint defense of females, so that dispersal is essentially forced upon females (Mitani et al. 2000; Watts 1998; Wrangham 1993), but other reasons for female dispersal in primates, such as inbreeding avoidance or abduction, must exist (Hammond et al. 2006). In other species, including gorillas and some colobine monkeys, social benefits of female dispersal can be decisive and thereby explain dispersal by both sexes (Steenbeek et al. 2000; Steenbeek and van Schaik 2001; Stokes et al. 2003; Watts 1992). Females of these species are faced with an unusually high infanticide risk and therefore associate with males that provide effective protection. Old, sick or injured males can no longer provide this form of social service effectively, so their groups dissolve because females desert them in search of new, more-powerful protectors. Whether dispersal decisions in primates with bisexual dispersal are also affected by ecological factors remains to be studied in detail. In summary, then, the occurrence of spatio-temporal clustering or permanent association of closely related individuals in primates is ultimately a function of speciesspecific social organization and sex-specific dispersal patterns, which, in turn, are primarily determined by reproductive strategies and characteristics of key resources.

11.5 Genetic Structure of Primate Societies Traditionally, behavioral observations and demographic data, which were collected on known individuals living in wild populations over years or even decades, were used to characterize social organization, to determine associated migration patterns

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and to make inferences about the genetic structure of the respective species (Silk 2002). Nowadays, it is possible to determine genetic structure, using DNA isolated from blood, tissue, hair or fecal samples (Catzeflis 1991; Kohn and Wayne 1997). With genetic data, it has become possible to validate conclusions of earlier, indirect studies, as well as to reveal hitherto hidden genetic structures. Because a complete review of primate population genetic studies is beyond the scope of this chapter, I will summarize selected studies on solitary, pair- and group-living species below, to generate a preliminary assessment of the range of interspecific variation (Table 11.1). In solitary nocturnal lemurs (Microcebus murinus and Mirza coquereli), complex genetic structures exist, despite or because of their solitary social organization (Fredsted et al. 2004, 2005; Kappeler et al. 2002; Wimmer et al. 2002). In both species, the majority of females is philopatric and lives in close spatial association with close kin. Specifically, females sharing a mitochondrial haplotype are spatially clumped within a local population and form stable daytime sleeping groups (Wimmer et al. 2002). Most males, in contrast, leave their natal area around the time of sexual maturity (Fredsted et al. 2005; Radespiel et al. 2003). In Microcebus murinus, females of a sleeping group also raise their offspring communally (Eberle and Kappeler 2006), suggesting that kin selection is structuring this aspect of their behavior. In Mirza coquereli, however, females rarely interact and never form sleeping groups, so that the adaptive consequences of kin clusters remain obscure (Kappeler et al. 2002). Fat-tailed dwarf lemurs (Cheirogaleus medius) are presently the only pair-living primate species, for which population genetic structure has been analyzed (Fredstedt et al. 2007). A comparison of two populations living about 3km apart revealed no evidence for spatial clustering of same-sexed individuals with identical mitochondrial haplotypes within each of two subpopulations but significant clustering between them. Moreover, both sexes showed equal variances in the number of individuals representing each haplotype, as well as equal levels of aggregation of identical haplotypes, suggesting that both sexes disperse from their natal area. There is a possibility of behavioral and social flexibility in this species, because we documented pronounced differences in density and sex ratio between the two subpopulations. Thus, as predicted, males and females of this socially monogamous species exhibit natal dispersal. Offspring from the previous year may stay with their parents, but helping-at-the-nest has not been reported (Fietz et al. 1999). Redfronted lemurs (Eulemur fulvus rufus) live in groups of up to ten adult males and females. The core of their groups is composed of 2–4 closely related adult females with identical mitochondrial haplotypes (Wimmer and Kappeler 2002). Immigrated males typically have divergent mt-haplotypes and are less closely related among each other. Interestingly, these group-living primates rarely form agonistic alliances, and both sexes defend their territories against neighboring groups (Pereira and Kappeler 1997), so that the consequences of close genetic relatedness among females are also not apparent in cooperative territorial defense (see also Nunn and Deaner 2004). Even more strikingly, adult females regularly attack and evict maturing female kin (Vick and Pereira 1989); a form of social behavior completely at odds with kin-selection theory (see also Pereira and Leigh 2003).

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In New World marmoset monkeys (Callithrix jacchus), 1–2 closely related reproductively active females also form the core of small bisexual groups. However, adult females, as well as the majority of males, regularly migrate between groups (Nievergelt et al. 2000). On average, females are more closely related among each other than males, who cooperatively help raise all offspring of a group (Goldizen 1987). A similar pattern has been described for tamarins (Saguinus mystax) (Huck et al. 2005). In red howler monkeys (Alouatta seniculus) males and females can either stay in their natal group or disperse from it (Pope 1998). As a result, the average degree of relatedness among group members is relatively low. A widespread lack of female kin-bonding in other New World primates has been recognized (Strier 1999), but the genetic structure of their populations has not been studied yet. Long-tailed macaques (Macaca fascicularis) represent the typical Old World monkey with female philopatry and male dispersal. Dyads of adult males are, on average, unrelated, whereas the average degree of relatedness among females corresponds to that of cousins (de Ruiter and Geffen 1998). In addition, every group contains several matrilines, with members of high-ranking matrilines exhibiting a higher degree of average relatedness than lower-ranking matrilines, presumably because members of high-ranking matrilines share more paternal alleles as a result of the alpha male to mate preferentially with high-ranking females. In savannah baboons (Papio cynocephalus) in Kenya similar patterns, albeit lower average coefficients of relatedness, were found (Altmann et al. 1997). How the genetic structure of female-bonded primates is by-and-large reflected in predicted kin-biased patterns of grooming and other forms of social support has been reviewed by Silk (2002). In chimpanzees (Pan troglodytes), most females emigrate from their natal group upon reaching sexual maturity, whereas males are philopatric and cooperatively defend their home range against neighboring groups. Genetic studies in two populations yielded divergent results. Based upon long-term behavioral observations and demographic data it was expected that males should be more closely related among each other than females. This prediction was confirmed in a population in Gombe (Tanzania), which was in turn used to explain male cooperative behavior (Morin et al. 1994). Another study in Tai forest (Ivory Coast) revealed, however, that males within a community are on average not more closely related to each other than are females (Vigilant et al. 2001). In every group, the average coefficient of relatedness among males was slightly, but significantly, higher. A re-analysis of the Gombe data with more stringent assumptions led these authors to the same conclusion about the Tanzanian population (Vigilant et al. 2001). Interestingly, the average difference in relatedness among chimpanzee groups in Tai forest was significant, suggesting that chimpanzees have on average more relatives within their group than outside of it. This pattern may explain the very hostile relations among neighboring chimpanzee groups. However, there is no obvious genetic basis or explanation for the highly cooperative behavior among males within a group. In bonobos (Pan paniscus), males are also the philopatric sex (Eriksson et al. 2006). Compared to chimpanzees, however, bonobo females are organized into large sub-groups, within which food sharing, agonistic support, as well as intense

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affiliative and homosexual behavior is common (White 1996; White and Burgman 1990). This level of cooperative behavior among females is not predicted by kinselection theory, however. Genetic studies of the degree of relatedness revealed that it is similarly low in males and females (Gerloff et al. 1999). The pronounced social behavior and cooperation among bonobo females can therefore also not be explained with kin-selection theory. In summary, the social behavior of primates for which population genetic data exist follows predictions of kin-selection theory in some cases (e.g., Microcebus, Macaca, Papio), whereas there is no congruence between the observed social organization or social structure and the genetic structure in other species (e.g., Mirza, Eulemur, Pan). This is a strong argument for additional, comparative studies in additional populations and species that should include members of all radiations and social systems. Moreover, the postulated correlation between sex differences in average degrees of relatedness and the frequency and intensity of cooperative behavior is at best weak, so that additional studies of social behavior of individuals with known pedigree are required to better characterize this relationship. Finally, this mismatch between predictions of kin-selection theory and empirical evidence underlines the need for more explicit consideration of additional social and ecological determinants of social behavior. This is the realm of the socioecological model.

11.6

Consequences for Social Behavior

The socioecological model (Fig. 11.1) provides a set of predictions about the interactions between genetic and ecological factors in the evolution of social structure in primates and other mammals (van Schaik 1989; see also Davies 1991; Linklater 2000). A logical starting point of this model is the assumption that female reproductive success, in contrast to that of males, is not limited by the number of mates, but rather access to resources, which are allocated to gestation and lactation (Emlen and Oring 1977; Trivers 1972; Williams 1966). Access to and competition for resources is therefore of greatest priority for female primates and subject to intense selection. Predation risk features prominently as a second important ecological determinant of social behavior. Specifically, group-living in diurnal species was favored because it decreases predation risk (van Schaik 1983): gregarious species can detect predators earlier and their per capita predation risk is significantly reduced, especially in small groups (Treves 1999). Feeding competition within groups is an unavoidable social consequence of grouping and leads to variation in social structure. The local competitive regime in turn is dependent on characteristics of main food resources, such as their size, spatial distribution and defendability, and has two distinct components (Koenig 2002; Sterck et al. 1997). When food patches, relative to group size, are of intermediate size, spatially clumped and economically defendable against conspecifics, they facilitate direct contest competition. Contest competition occurs whenever individuals can exclude others by use of force from a resource. Other combinations of

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Fig. 11.1 Schematic summary of evolutionary determinants of primate social structure, separated by sex-specific dyads (see text for details)

resource characteristics lead to scramble competition, which is characterized by the fact that that some individuals lose access to a resource because others have already exploited it. Both types of competition occur both within and between groups, so that every primate female is exposed to a combination of contest and scramble competition within and outside her group (van Schaik 1989). The intensity of scramble competition is primarily dependent on group size; the more members a group has, the more intense is scramble competition among them. The intensity of contest competition, in contrast, primarily reflects the effects of dominance; whenever pronounced, steep dominance hierarchies exist, this type of competition is most intense between high and low-ranking individuals. The intensity of between-group competition is primarily a function of population density and resource distribution; whenever many groups compete for access to widely dispersed resources, this type of competition is most intense. However, competition within groups is always stronger than between groups, and therefore of greater evolutionary significance (van Schaik 1989). The consequences of one of the four competitive regimes for female social relationships are being modulated by three non-independent variables: philopatry, nepotism and despotism (Sterck et al. 1997). Their combination yields four realistic scenarios. In resident-nepotistic groups, females are philopatric, support their relatives and cooperate with them in other ways, and they exhibit despotic dominance relations as a result of intense within-group contest competition. In emigrant-egalitarian groups, females move among groups, form no agonistic

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coalitions and do not cooperate in other contexts. They also lack stable, linear dominance hierarchies as a result of weak within-group contest competition. Whenever feeding competition between groups is pronounced, resident-egalitarian groups are favored, which are characterized by female philopatry and a lack of dominance relations and coalitions. Finally, whenever feeding competition is pronounced within as well as between groups, tolerant resident-nepotistic groups with female philopatry, clear dominance relations, coalitions and pronounced tolerance of dominants towards subordinates are favored. A more detailed characterization of these competitive regimes and their underlying logic can be found in van Schaik (1989), Sterck et al. (1997) and Koenig (2002). The socioecological model has been extended in important ways in the last years because the original model was focused on ecological determinants of femalefemale relationships only. By considering social variables as well, intersexual and male-male relationships could be also included (van Schaik 1996). One additional assumption is that infanticide risk emanating from strange males and other forms of sexual coercion have favored the evolution of permanent male-female association (van Schaik and Kappeler 1997). This permanent association between the sexes goes well beyond brief mating encounters characteristic of many other mammals. Reasons for this primate idiosyncrasy may have to do with primate’s slow life histories and their type of parental care (van Schaik 2000b). Because the adult sex ratio is highly variable among groups and species, intersexual relationships across primates are highly diverse (Kappeler 1999; Nunn and van Schaik 2000). Male relationships are generally less variable (van Hooff 2000, van Hooff and van Schaik 1994). They are characterized by mating competition and a lack of cooperation; presumably because they compete for a resource that cannot be shared: fertilizable eggs. Only in a few exceptional cases we find cooperative male defense of females and the attendant relaxed social relationships among males (van Hoof and van Schaik 1994). Several aspects of primate social relationships are additionally influenced by interactions between ecological and life-history variables (Kappeler et al. 2003), but this area, as well as inter-sexual and male-male relationships require much additional theoretical and empirical work.

11.7

Discussion

This review of current evolutionary models of primate social behavior revealed that (1) empirical research is well behind theoretical developments, (2) the existing genetic data have identified some significant deviations from theoretical expectations of kin-selection theory, and (3) explanations of male-male and intersexual relationships are based on still preliminary theoretical foundations. However, the underlying model is firmly rooted in evolutionary theory and has convincing explanatory power for female social relationships (Koenig 2002; Sterck et al. 1997). It will therefore be interesting to follow the integration of the results of additional socioecological studies of additional (non-Old World monkey) species

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living under different ecological conditions, as well as pair-living (Schülke 2003) and solitary species (M. Dammhahn unpubl. data). With respect to kin-selection theory, the existing data speak primarily on the consequences of kinship on dominance and coalitionary behavior. There are studies addressing other aspects of cooperative behavior, such as cooperative hunting, male mate defense coalitions, cooperative infant care and social tolerance, for example in the context of food sharing and their underlying proximate and evolutionary mechanisms (Bercovitch 1988; Boesch et al. 2006; Chapais 2001; Chapais et al. 1997, 2001; Garber 1997; Pope 1990; Silk 2002a; Walters and Seyfarth 1987). This body of work has recently been reviewed elsewhere (van Schaik and Kappeler 2006). Studies of altruism in primates continue to be hampered by two fundamental problems. First, it is neither easy to identify cooperative behavior as such, nor to determine the exact costs and benefits for the lifetime reproductive success of the actor and recipient. Second, it is difficult, presumably also for the animals themselves, to determine the exact degree of relatedness among all possible dyads in a social unit. The problem of kin recognition is especially evident with respect to paternal relatedness (Silk 2002a). In polygynous primate mating systems, reproductive skew in favor of one or a few high-ranking males is common, so that cohorts of infants share identical alleles from the same father. There is some evidence that paternal relatedness can affect social behavior; in rhesus macaques (Macaca mulatta), young females affiliated much more with paternal half sibs than with non-relatives of the same peer group (Widdig et al. 2001). Savannah baboons (Papio cynocephalus) can also detect kinship through the paternal line and adjust their social behavior accordingly (Alberts 1999; Smith et al. 2003). Genetic similarity through the paternal line therefore needs to be considered in future studies of the effects of kinship on social behavior more explicitly in other taxa as well. Additionally, a number of recent theoretical papers have warned against an overinterpretation of the effects of kin selection on social structure (Clutton-Brock 2002; Griffin and West 2002; West et al. 2001; 2002). Accordingly, it is not sufficient to demonstrate a high degree of relatedness between the members of a dyad in order to ascribe an altruistic act to kin selection because the beneficial effects of kin selection can be reduced by the effects of competition among relatives. Moreover, an apparently altruistic act can also yield important direct benefits for the actor that are difficult to recognize. More generally, the costs and benefits of a particular behavior need to be identified more precisely and their evaluation against a particular background of ecological conditions needs to be emphasized more (Griffin and West 2003). However, from a primatological perspective, it should also be kept in mind that most refinements of existing theory focus on cooperative breeders, which are a small minority among primates. Finally, a number of other mechanisms, such as reciprocity, mutualism, biological market effects and friendship (Clutton-Brock 2002; Grinnell et al. 1995; Hemelrijk and Ek 1991; Noe and Hammerstein 1994; Rapaport 2001; Silk 2002b; de Waal 1989) have been invoked to explain cooperation among unrelated individuals, but there is no reason why they should not also operate among kin. Such broader approaches in a second generation of sociogenetic studies may contribute to more comprehensive explanations of the full range of variation in

Callithrix jacchus Alouatta seniculus Macaca fascicularis Papio cynocephalus Pan troglodytes

Marmoset monkey Red howler

Philopatric

Group

Group

Group

Group

Philopatric

Group

Philopatric & Migrate Philopatric & Migrate Philopatric

Philopatric

Solitary

Group

Philopatric

Solitary

Migrate Migrate Bonobo Pan paniscus Group Migrate For every species, its social organization, the modal migration behaviour of same-sex dyads is presented

Longtailed macaque Savanna baboon Chimpanzee

Microcebus murinus Mirza coquereli Eulemur fulvus

Grey mouse lemur Coquerel’s dwarf lemur Redfronted lemur

Table 11.1 Summary of selected studies of genetic structure in primates Social Name organization Females

0.08 0.003–0.05 −0.02 both sexes and the

−0.02

0.14

−0.2

−0.10

0.24–0.40

−0.05 0.2

0.1–0.27

0.05

−0.08

rM

Philopatric 0.22 Philopatric −0.01–0.15 Philopatric 0.05 average coefficient of relatedness (r)

Migrate

Philopatric & Migrate Migrate

Migrate

−0.06 0.5 0.27–0.43

Migrate

Migrate

Migrate

Males

0.27–0.7

−0.02

−0.05

rf

Morin et al. 1994 Vigilant et al. 2001 Gerloff et al. 1999 (or its range) between

de Ruiter and Geffen 1998 Altmann et al. 1996

Pope 1998

Nievergelt et al. 2000

Wimmer and Kappeler 2002

Kappeler et al. 2002

Wimmer et al. 2002

Reference

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primate social behavior, including the existence of cooperation in species where it is not predicted by genetic structure, as well a lack of cooperation or even fatal aggression among kin. The broad comparative and interdisciplinary approach advocated by the contributions to this volume ought to be helpful in this endeavor. Acknowledgements I thank Judith Korb and Jürgen Heinze for the invitation to contribute to this volume, for their comments on this contribution, and for their patience.

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van Hooff JARAM (2000) Relationships among non-human primate males: a deductive framework. In: Kappeler PM (ed) Primate males: causes and consequences of variation in group composition. Cambridge University Press, Cambridge, pp 183–191 van Hooff JARAM, van Schaik CP (1994) Male bonds: affiliative relationships among nonhuman primate males. Behaviour 130:309–337 van Schaik CP (1983) Why are diurnal primates living in groups? Behaviour 87:120–144 van Schaik CP (1989) The ecology of social relationships amongst female primates. In: Standen V, Foley RA (eds) Comparative socioecology. Blackwell, Oxford, pp 195–218 van Schaik CP (1996) Social evolution in primates: the role of ecological factors and male behaviour. Proc Brit Academy 88:9–31 van Schaik CP (2000a) Infanticide by male primates: the sexual selection hypothesis revisited. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge van Schaik CP (2000) Vulnerability to infanticide by males: patterns among mammals. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 61–71 van Schaik CP, Kappeler PM (2003) The evolution of social monogamy in primates. In: Reichard UH, Boesch C (eds) Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge University Press, Cambridge, pp 59–80 van Schaik CP, Kappeler PM (1997) Infanticide risk and the evolution of male-female association in primates. Proc R Soc Lond B 264:1687–94 van Schaik CP, Kappeler PM (2006) Cooperation in primates and humans: closing the gap. In: Kappeler PM, van Schaik CP (eds) Cooperation in primates and humans. Springer, Berlin Heidelberg New York, pp 1–19 van Schaik CP, van Hooff JARAM (1983) On the ultimate causes of primate social systems. Behaviour 85:91–117 Vick LG, Pereira ME (1989) Episodic targeting aggression and the histories of lemur social groups. Behav Ecol Sociobiol 25:3–12 Vigilant L, Hofreiter M, Siedel H, Boesch C (2001) Paternity and relatedness in wild chimpanzee communities. Proc Natl Acad Sci USA 98:12890–12895 Walters JR, Seyfarth RM (1987) Conflict and cooperation. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 306–317 Waser PM, Jones WT (1983) Natal philopatry among solitary mammals. Q Revi Biol 58:355–390 Watts DP (1990) Ecology of gorillas and its relation to female transfer in mountain gorillas. Int J Primatol 11:21–45 Watts DP (1992) Social relationships of immigrant and resident female mountain gorillas. I. Malefemale relationships. Am J Primatol 28:159–182 Watts DP (1998) Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda. Behav Ecol Sociobiol 44:43–56 West SA, Murray MG, Machado CA, Griffin AS, Herre EA (2001) Testing Hamilton’s rule with competition between relatives. Nature 409:510–513 West SA, Pen I, Griffin AS (2002) Cooperation and competition between relatives. Science 296:72–75 White FJ (1996) Pan paniscus 1973 to 1996: twenty-three years of field research. Evol Anthropol 5:11–17 White FJ, Burgman MA (1990) Social organization of the pygmy chimpanzee (Pan paniscus): multivariate analysis of intra-community associations. Am J Phy Anthropol 83:193–201 Widdig A, Nürnberg P, Krawczak M, Streich WJ, Bercovitch FB (2001) Paternal relatedness and age proximity regulate social relationships among adult female rhesus macaques. Proc Natl Acad Sci USA 98:13769–13773 Williams GC (1966) Adaptation and natural selection. Princeton University Press, Princeton

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Wilson DS, Dugatkin LA (1997). Group selection and assortative interactions. Am Nat 149:336–351 Wimmer B, Kappeler PM (2002) The effects of sexual selection and life history on the genetic structure of redfronted lemur, Eulemur fulvus rufus, groups. Anim Behav 63:557–568 Wimmer B, Tautz D, Kappeler PM (2002) The genetic population structure of the gray mouse lemur (Microcebus murinus), a basal primate from Madagascar. Behav Ecol Sociobiol 52:166–175 Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300 Wrangham RW (1987) Evolution of social structure. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 282–297 Wrangham RW (1993) The evolution of sexuality in chimpanzees and bonobos. Human Nature 4:447–480 Wynne-Edwards V (1962) Animal dispersion in relation to social behaviour. Oliver & Boyd, Edinburgh

Chapter 12

The Ecology of Social Life: A Synthesis Judith Korb(* ü ) and Jürgen Heinze

Abstract All the chapters of this book highlight to some extent the importance of kinship in the evolution of social life throughout the animal kingdom. They also accentuate that variation in genetic relatedness alone is not sufficient to explain the occurrence or details in the organization of social life. A comparative summary of the ecological and demographic factors favoring social life reveals some striking patterns of correlated traits (sociality syndromes). Accordingly, three types of sociality can be distinguished: (i) Aphids, thrips, wood-dwelling termites and the naked mole rat are all groups of totipotent individuals without intensive alloparental care protected by altruistic defenders. They have a long-lasting bonanza-type resource and a safe nest that offers the opportunity of inheriting the natal breeding position. (ii) Social Hymenoptera and non-wood dwelling termites with sterile or subfertile workers are characterized by intensive, altruistic alloparental care that usually involves progressive food provisioning. (iii) Cooperatively breeding vertebrates and social Hymenoptera with totipotent workers (e.g., wasps and queenless ants) take an intermediate position between class (ii) and class (i). Helpers here can gain indirect fitness benefits through alloparental care as well as direct benefits through inheriting the breeding position or by founding an own nest.

12.1

Kin Selection, the Key to the Evolution of Social Life

Cooperation, altruism, and sociality have long been considered as major forces in evolution, albeit the attention they have received relative to that paid to competition, parasitism, and other forms of antagonism has varied over the last 150 years from undue disregard to similarly unjustified preponderance (see Chap. 1).

Judith Korb, Department Biology I, University of Regensburg, 93040 Regensburg, Germany [email protected]

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Comparable ups and downs have characterized the importance of kin selection as the key explanation for the evolution of altruism. While it needed almost a decade before W.D. Hamilton’s inclusive fitness theory (Hamilton 1964) became more widely known, let alone accepted, among biologists (e.g., Hamilton 1996), some 40 years later few researchers doubt its fundamental importance. Though newgroup or multilevel selection has repeatedly been spearheaded as seemingly nonkinship-based alternatives for kin-selection theory (Alonso and Schuck-Paim 2002; Wilson and Hölldobler 2005; Wilson 2005), such approaches often appear to suffer from common and long-lasting fallacies (Dawkins 1979; Foster et al. 2006). Consequently, proponents of kin-selection theory have repeatedly emphasized the critical role of kinship in the evolution of altruism (Foster 2006; Foster et al. 2006; see Chap. 1). As can be told from the chapters in the present book, studying sociality over a wide range of animals strongly supports this view. If helping reduces the helper’s direct fitness it is essential that helping is directed towards relatives, because otherwise the ‘genes’ underlying the helping trait would be propagated less efficiently to the next generation than those of unrelated, selfish individuals, which do not help. New group-selection models (‘multilevel selection’) therefore do not provide an alternative to kin selection (Hamilton 1975; Queller 1992; Frank 1998; Chap. 1), though, as will be explained in more detail below, they present a promising way of investigating social phenomena. They consider groups as an additional unit of selection with selection simultaneously occurring at different levels, e.g., between individuals in the group and between groups, and the strength of selection depending on the co-variance of genetic traits at the different levels (see also Price 1970; Hamilton 1975; Wilson 1975; Wade 1978a; Sober and Wilson 1997). The predominant factor that increases this covariance, decreases conflict within groups and strengthens selection among groups is the common ancestry of group members. Though other factors, such as green-beard alleles or habitat heterogeneity, may in principle also lead to a positive assortment of altruists (Dawkins 1976; Wilson and Dugatkin 1997; Pepper and Smuts 2002; Axelrod et al. 2004), they appear to be rare in nature (Grafen 2006). Because in nature, the co-variance of genetic traits mostly, if not exclusively, relies on common ancestry, new group selection and kin-selection models become equivalent (Wade 1978b; Grafen 1984; Queller 1992). Both make the same predictions about which conditions favor altruism, but differ in their emphasis on different variables. In kin-selection models, relatedness is the most obvious variable and also the one that can be quantified most easily. Other factors are less explicitly hidden in the cost and benefit terms in Hamilton’s famous inequality (Hamilton 1964). In contrast, the new groupselection models accentuate between- versus within-group selection and thus focus on group level phenomena, such as the effects of group size. Kin selection becomes a special form of new group selection specifically applicable for interactions among conspecifics, whereas new group-selection models more generally include also the evolution of cooperative interactions between species, as in symbiosis (e.g., Frank 1997; Wilson 1997).

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Kin-selection (and, correspondingly, new group-selection) models similarly are applicable to explain the evolution of cooperation (mutual benefit; sensu Chap. 1), i.e., when interacting partners receive direct benefits from their association that are greater than the resulting costs. In contrast to altruism, there is no loss in direct reproduction. Kinship may nevertheless be important also in this context as it reduces conflict among the interacting partners and aligns their evolutionary interests. Cheating is therefore less likely to evolve. Thus, Hamilton’s rule describes both the evolution of cooperation and that of altruism and either direct benefits or indirect benefits ensure that the inequality is fulfilled. Only if the costs of an action are smaller than its benefits (direct in the case of cooperation and indirect in the case of altruism) will it be favored in evolution.

12.2 12.2.1

Common Patterns Among Social Organisms Importance of Kinship

All chapters of this book emphasize the importance of kinship in the evolution of social life throughout the animal kingdom. The same appears to apply to those social organisms that are not covered in this book, such as social microorganisms (Crespi 2001; West et al. 2006; Foster et al. 2007), ambrosia beetles (Kent and Simpson 1992; Peer and Taborsky 2007) and communal spiders (Whitehouse and Lubin 2005). Cooperation and altruism among conspecific individuals usually occur in kin groups, mainly families, when offspring delay maturity and stay at the natal nest. At the same time, the chapters accentuate that variation in relatedness alone is not sufficient to explain the occurrence or details in the organization of social life. Given that Hamilton’s rule is composed of three variables, this might at first glance appear trivial. Yet, ecological costs and benefits of cooperation have often been disregarded in standard textbooks, e.g., when the evolution of eusociality in social Hymenoptera is erroneously attributed to haplodiploidy alone, or when it is stated that the degree to which altruistic behavior should be extended toward other individuals depends only on the relatedness between helper and recipient. Examples from this book show that variation in relatedness alone is not sufficient to explain the occurrence or pattern of helping behavior in the stenogastrine wasp, Liostenogaster flavolineata (see Chap. 4) or the occurrence of ‘workers’ in the basal termite, Cryptotermes secundus (see Chap. 6). Across species of aphids, the occurrence of altruistic soldiers does not correlate with relatedness levels and, although all aphids are clonal, only a few species have soldiers (see Chap. 2). Furthermore, it cannot explain cooperative breeding in some bird species, where helpers aid in raising unrelated young (see Chap. 8). Similarly, variation in the social organization of ants (see Chap. 6) and primates (see Chap. 11) can hardly be explained by relatedness alone. Variation in

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relatedness does neither explain variation in worker reproduction among ant species (see Chap. 6; Hammond and Keller 2004; but see Wenseleers and Ratnieks 2006) nor the occurrence of dispersal patterns and composition of groups in primates (see Chap. 11). Whereas kinship can easily be quantified using genetic markers—though its exact meaning and the appropriate level of analysis may occasionally remain obscure to empiricists (Creel 1990; Lucas et al. 1996; Queller 1996)—ecological factors as hidden in the c and b terms of Hamilton’s rule are inherently difficult to measure.

12.2.2

Importance of Ecological Factors

A comparison of the different chapters reveals a number of ecological factors that repeatedly show up as vital for the evolution of sociality. Previous syntheses have similarly aimed at identifying fundamental ecological and life-history traits (Alexander 1974; Emlen 1982; Stacey and Ligon 1991; Reeve 1998; Johnstone 2000; Whitehouse and Lubin 2005), and consequently some overlap exists between earlier work and our overview in Table 12.1. In the following section, we summarize the factors that appear to be important, and discuss them in the context of previously proposed hypotheses. Corresponding to the “ecological constraint hypothesis” (Emlen 1982, 1997), three factors favor the offspring’s staying at the parental nest: (i) limitation of nesting sites, (ii) high dispersal-related mortality costs, and (iii) demographic factors like group size. (i) Limitation of nesting sites has been shown to play a prominent role for the occurrence of helpers in birds (Hatchwell and Komdeur 2000; Dickinson and Hatchwell 2004; Chap. 8) and was also suggested as important for the evolution of polygyny and high reproductive skew in ants (e.g., Bourke and Heinze 1994; Chap. 6). In contrast, providing additional nests did not affect the occurrence of helping behavior in the stenogastrine wasp L. flavolineata (Field et al. 1998), which, together with the availability of vacant nests in natural populations, suggests that nest site limitation is less important in the evolution or maintenance of helping in this species. (ii) High mortality during dispersal seems to be a common phenomenon in all social organisms, especially thrips, termites, and naked mole-rats. In social Hymenoptera (and several termites), it might have selected for the founding of new societies by reproductives leaving the parental colony with a group of workers in a process called swarming or budding. In microorganisms, the dispersal phase is similarly the stage during which individuals ‘behave socially’ and form groups, and apparently they preferentially aggregate with clonemates (Mehdiabadi et al. 2006). Sociality may also be associated with dispersal in social mammals, albeit to a lesser extent. For example, male lions can form alliances that leave the natal group and have a higher chance of taking over female

− − (+) −

+ + +

+ + +

+ −

Bonanza type resource Fortressc defense Predator/parasite defensed Inbreeding Inheritancef Nepotismg − + −

− − +

Haplodiploidy − − + + − − + : polygyny polyandry − −e −

Haplodiploidy + : polygyny + + +

Ants2

− − −

+ + + +

Diploid

Birds3

OP: + MP: −(+) − OP: + MP: −(+) + + +

OP: + MP: − OP: + MP: − OP: − MP: +

− OP: + MP: + + OP: − MP: +

Diploid

Termites OP1 MP2

+ +

+ + +

−

− +

Diploid

Mole rats1

− −/+ +

−/+ −/+ − limited due to lactation − −/+ +

Diploid

Mammals1,3

Three sociality syndromes can be identified, which are marked by different indices: type (i):1; (ii)2; (iii):3. Type (i) species are characterized by a bonanza-type food resource, fortress defense, inheritance opportunities, and the possibility of inbreeding, while allofeeding is of low importance. Type (ii) species are characterized by allofeeding and absence of a bonanza-type resource and fortress defense with inbreeding avoidance and generally few opportunities to inherit the natal breeding position. Type (iii) species have an intermediate position with allofeeding being important, but having the opportunity to inherit the natal breeding position, although this might be limited by the necessity to avoid inbreeding. Cooperatively breeding mammals have species that belong to type (i), while others belong to type (iii). +: important factor; −: factor with low importance (for inbreeding: − indicates strict inbreeding avoidance); OP: wooddwelling, one-piece nester termites; MP: non-wood-dwelling, multiple-pieces nester termites. a Mainly based on results for Liostenogaster flavolineata b Foraging and allofeeding offer the opportunity for load lightening of the breeders; local resource competition is prevented by increasing the food intake c Defense is mainly directed against competitors that try to invade/occupy the nest d Defense is mainly directed against predators and parasites e Except for species with gamergates where nest inheritance is common f Individuals can regularly gain direct fitness in the nest by inheriting the breeding position g Nepotism, not true kin discrimination, sensu Grafen (1990)

− − +

+ + +

− − + −

Haplodiploidy − − − +

Habitat saturation Dispersal costs Demography Foraging/Allofeedingb

Haplodiploidy − + + −

Bees / Wasps2 Wasp3, a

Clonal

Thrips1

Genetic

Aphids1

Table 12.1 Factors considered important for favoring the evolution of sociality and group living

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prides than solitary males (Heinsohn and Packer 1995). In wild dogs, spotted hyenas, and primates, large groups can split to subsequently occupy two territories (Solomon and French 1997). Even after dispersal, the small chance that an individual will survive long enough to rear offspring through maturity favors helping over independent reproduction in primitively eusocial wasps (Gadagkar 1991; Queller and Strassmann 1998; Field et al. 2000; see Chap. 4). (iii) Finally, demography, i.e., population density, has been shown to explain some variability in the degree of altruism. As predicted by a model, thrips and aphids produce more soldiers when their density in the gall is high and birth rate is low (see Chaps. 2 and 3). In such situations, the costs of producing a soldier compared to a sexual are low because groups exist at their carrying capacity. In the stenogastrine wasp L. flavolineata and the termite C. secundus colony size influences the degree of altruism and cooperation, respectively. Termites are more likely to develop into dispersing sexuals when colony size is high and hence the probability to inherit the colony is low (see Chap. 7). Wasps work less hard if they are high up in the colony’s dominance hierarchy and so have a good chance of becoming a reproductive in the future, and if the group they might to inherit is larger (Field et al. 2006). The position in the queue similarly influences the amount of alloparental care provided in several birds (Koenig and Dickinson 2004). The influence of demographic factors in ants, bees, and mammals is less clear, but Tsuji (2006) has recently demonstrated the importance of population density and growth rate for the evolution of colony characteristics, such as queen number, in ants. Corresponding to the “benefits of philopatry hypothesis” (Stacey and Ligon 1991), four factors favor sociality through individuals gaining inclusive fitness at their natal nests: indirect fitness through (i) alloparental brood care and (ii) defense of relatives against parasites and predators; (iii) direct fitness through nest inheritance or increased experience; and (iv) both, direct and indirect fitness, through the monopolization of a “bonanza-like” food source against competitors. (i) Indirect fitness benefits through alloparental brood care appear to be particularly important in social Hymenoptera, higher termites, and several birds. In mammals, the ability to care directly for the offspring of others is often restricted by the need of having lactating females (Solomon and French 1997). Thus, nonreproducing helpers in mammals can only gain indirect fitness benefits when providing food for the parents increases their respective reproductive success or when they play an important role in provisioning young after weaning. Hence, the potential to provide care, the potential to increase the reproductive success of the breeder by helping and load lightening, and progressive food provisioning are facilitators of alloparental brood care. The rarity of sociality in sphecid wasps compared to bees might thus be explained by their inability to provide help because of a different type of food provisioning (see Chap. 5). The type of food is similarly essential for the occurrence of altruistic helping in termites. In wood-dwelling termites, like C. secundus, the potential to reduce the workload of reproductives is small, as all individuals live within their food and extensive,

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costly foraging is not necessary (Korb 2007). In species in which nest and food are separated, individuals can considerably help the reproductives by providing the young with food that is costly to collect. A similar association between load lightening and helping is also found in birds (Heinsohn 2004). (ii) Indirect fitness can also be gained by efficiently defending relatives against predators and parasites. This seems to play a role in several cooperatively breeding mammals where non-reproducing offspring stay at the nest as ‘guards’ that warn young by alarm calls, as in the case of Belding’s ground squirrel (Sherman 1977) (although it is questionable whether these calls are always altruistic, i.e., associated with costs to the caller; for meerkats it has been shown that they confer direct fitness benefits; Clutton-Brock et al. 1999). Defense seems to be less important in most cooperatively breeding birds, although several exceptions may exist. For example, alarm calls are a common phenomenon in Arabian babblers (Zahavi 1990). In insects, predators (and especially parasites) constitute an important selection pressure although it strongly depends on the type of parasite whether group living can offer protection (see Chap. 5). In social Hymenoptera, parasitism has been invoked to explain variation in the structure of societies, in particular mating frequency. According to the “diversity against parasites hypothesis”, genetically more diverse colonies are better protected against parasites and pathogens (Sherman et al. 1988; Baer and Schmid-Hempel 1999; Brown and Schmid-Hempel 2003). In ants, polygyny seems to offer better protection against social parasites, such as slave-making ants, due to larger colony sizes and a higher chance that one queen survives a slave-raid (see Chap. 6). In contrast, social life in aphids, thrips, termites, the stenogastrine wasp L. flavolineata and naked mole rats, in general, seems to provide protection more against intraspecific competitors than predators or parasites (see below; Cronin and Field 2007). (iii) Direct fitness gains through nest inheritance can potentially play an important role in species with totipotent helpers / workers, such as those social Hymenoptera, where workers can mate and produce both female and male offspring, wooddwelling termites, aphids, and thrips in which soldiers can still reproduce, the naked mole-rat and cooperatively breeding vertebrates. In social Hymenoptera, such as monogynous ants, which build large colonies, nest inheritance plays a minor role, probably because the chance of inheritance is zero or negligible, and because parasites and pathogens accumulate in their nests. Additionally, in analogy to Metazoa that undergo a single-cell stage during embryogenesis, a single-queen founding phase might punish selfish genetic lineages (Heinze et al. 2001). Direct benefits arising from individuals acquiring skills in brood care, which later increase their own breeding success, seem restricted to some cooperatively breeding vertebrates with more complex behavior of brood care and brood provisioning (Komdeur 1996; Russell 2004). Incest avoidance often prevents inheriting the breeding position in cooperatively breeding birds and mammals, and the necessity to outbreed creates complicated dynamics in vertebrate groups and results in a high fluctuation of

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group members (Pusey and Wolf 1996; Emlen 1997; Koenig and Haydock 2004). Either the heir to the nest must be an alien or an offspring must find an unrelated mate. In contrast to social Hymenoptera, where inheriting queens are supposed to avoid inbreeding by mating with alien males (e.g., Hölldobler and Bartz 1985), considerable conflicts arise in social vertebrates and often lead to the breakdown of groups (Emlen 1997). In social Hymenoptera, alien males play only a transient role as they die shortly after mating (Boomsma et al. 2005). In social vertebrates, alien breeders remain in the group together with unrelated older offspring, with whom they compete for access to food etc. The resulting conflicts lead to the dispersal of unrelated older offspring or, in extreme cases, infanticide, as in lions and Hanuman langurs (Hrdy 1977; Pusey and Packer 1994), and certainly limit the benefits of nest inheritance. In termites, inbreeding seems to be less of a problem. Strikingly, the only social mammal with castes, the naked mole rat, shows considerable degrees of inbreeding (see Chap. 10). Although the benefits from nest inheritance have rarely been measured, they are probably very important factors for the evolution of sociality in the naked mole rat, social wasps and a few species of ants, where totipotent workers can inherit the natal breeding position when the current breeder dies. For the wood-dwelling termite C. secundus (Korb 2007) as well as some bird species, such as the Australian Magpie (Veltman 1989), where individuals stay at the nest and do not work, or for those birds where helpers raise unrelated offspring (Reyer et al. 1986; Dunn et al. 1995), staying for direct benefits apparently is the driving force of social life. (iv) Both direct and indirect benefits, which accrue to individuals through monopolization of a “bonanza-like” type of food, seem to be crucial for the evolution of social life in aphids, thrips, wood-dwelling termites and the naked mole rat. These species, together with spiders (Whitehouse and Lubin 2005) have in common that their nest is identical (aphids, thrips, wood-dwelling termites) or closely linked (naked mole rat, social spiders) with their food. This allows individuals to coexist over long periods without local resource competition and favors group-living in that the resource can be defended against competitors. Consequently, soldiers have evolved in most of these taxa, which defend the resource against competitors rather than the group against predators and parasites. Similar, but to a lesser extent, increased foraging efficiency and monopolization of resources also seem to favor group-living in some primates (see Chap. 11) and carnivores, such as wolves, wild dogs, foxes, and spotted hyenas (Gittleman 1989; Creel and Creel 1995).

12.3

Sociality Syndromes

A comparative summary of the ecological factors favoring social life reveals some striking patterns of correlated traits (Table 1). Accordingly, three types of sociality can be distinguished, each with a unique combination of ecological factors:

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(i) Aphids, thrips, wood-dwelling termites and the naked mole rat are all groups of totipotent individuals protected by altruistic defenders or soldiers. They monopolize a long-lasting bonanza-type resource, which supports the co-existence of many individuals without selection for dispersal (Hamilton and May 1977). The totipotent individuals do not provide intensive alloparental care, probably because food is easily accessible to all individuals and alloparental care cannot strongly alleviate the reproductive burden of breeders. Helpers seem to stay because the nest is a safe haven with plenty of food and a substantial possibility of inheriting the natal breeding position. The chances of founding an own nest independently are low due to high mortality risks during dispersal in an unfavorable environment. The only truly altruistic individuals in these groups are the defenders (soldiers), which mainly protect the resource against competitors and partly against predators. According to Queller and Strassmann (1998), such altruistic individuals can be called “fortress defenders”. Inbreeding, which regularly occurs in such societies, seems to play an important role, not necessarily through increasing relatedness, but through reducing relatedness asymmetries in the haplodiploid thrips (see Chap. 3) and stabilizing groups over longer periods as heirs do not have to mate with unrelated, alien partners (in contrast to vertebrates). (ii) Social Hymenoptera and non-wood dwelling termites with sterile or subfertile workers are characterized by intensive, altruistic alloparental care. They engage in costly helping with low chances of reproducing. Brood care usually involves progressive food provisioning, which is costly to the reproductives and can be ‘handed over’ to workers. Consequently, reproductives can concentrate on egg laying. (iii) Cooperatively breeding vertebrates and social Hymenoptera with totipotent workers (e.g., wasps and queenless ants) take an intermediate position between societies with altruistic, subfertile workers of class (ii) and those consisting of the totipotent individuals of class (i). Helpers can gain indirect fitness benefits through alloparental care as well as direct benefits through inheriting the breeding position or, in many cases, by founding an own nest. In vertebrates, group instability due to inbreeding avoidance, together with other factors such as their comparatively low fecundity, might be one explanation for the lack of large social vertebrate groups (with the exception of naked mole rats which show inbreeding; see Chap. 10). The ecological factors favoring alloparental care in totipotent workers are identical to those for subfertile workers of class (ii), namely the potential to provide costly help that frees the reproductives from provisioning their offspring. At the same time, one would expect that totipotent individuals are less altruistic or adjust their altruistic investment according to their chances to inherit the breeding position (Kokko and Johnstone 1999). Although not many data exist, those available suggest that they indeed do: depending, for instance, on their own rank in the society’s hierarchy, wasps and birds invest differentially in alloparental care (Field et al. 1999; Koenig and Dickinson 2004; Cant and Field 2005). Additionally, at least in some birds, totipotent workers seem to adjust

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their helping behavior to dispersal opportunities: when provided with extra nesting sites, helpers in the Seychelles warbler left the natal nest (Komdeur 1992; Komdeur et al. 1995). The comparatively small group sizes of coexisting totipotent workers might be explained by several factors: (i) The opportunity of founding independently, (ii) presumed decreasing benefit of helping with increasing group size (Michener 1964; Reyer 1984; Karsai and Wenzel 1998) and (iii) the limitation of food sources, which causes local resource competition. In queenless ants, where totipotent gamergates presumably are not capable of founding independently, group sizes are often much larger, which indicates that limited dispersal options force helpers to stay and leads to larger group size.

12.4

Future Perspectives

As this book demonstrates, social evolution is driven by a number of different ecological conditions, and three particularly important classes of selection pressures seem to emerge (Table 12.2). The knowledge of the ecological forces differs strongly between different types of animal societies as has especially been shown for social vertebrates. For social insects, clearly more ecological studies are needed to determine their importance (Boomsma and Franks 2006). The impact of ecological factors is hidden in the cost-and-benefit terms of Hamilton’s rule, which makes an easy quantification difficult. Applying a multilevel selection approach might therefore be fruitful. As mentioned above, it is equivalent to the kin-selection approach, but because it more clearly stresses parameters, such as group size, it might thus be helpful to obtain a more complete understanding of social phenomena (Foster 2006). While kinship has often been considered the most obvious and prominent parameter in Hamilton’s rule, multilevel selection also concentrates on the individual versus the group component of fitness. The latter is certainly of fundamental importance in social insects, because properties emerging through the interaction of individuals, such as thermoregulation, social homeostasis, and ecological dominance, are selected on the level of the “superorganismic” colony (Korb and Heinze 2004). Selection on colonies increases colony efficiency, partly at the cost of the interests of single individuals. Thus, the lack of true kin discrimination in social Hymenoptera or the widespread absence of worker reproduction is explained by the negative effect they would have on colony-level efficiency (Ratnieks 1988; Hammond and Keller 2004). However, our knowledge of the effects of group size or unpoliced worker egg laying on the overall reproductive success of a colony is surprisingly limited (but see Hartmann et al. 2003). Taking such group-level effects into account will certainly help to resolve apparent mismatches between predictions from kinship relations and the behavioral decisions of individual group members.

Type I

Naked mole-rat

Wood-dwelling termites

• Bonanza-type food • Fortress defense • Inheritance opportuntities • Inbreeding possible • No allofeeding Less altruistic immatures + Soldiers • Mainly direct fitness for most individuals, except few soldiers • Aphids • Thrips • Wood-dwelling termites • Naked mole-rat

Type III

Some ooperatively breeding mammals

• Most wasps • Cooperatively breeding birds • Some cooperatively breeding mammals Wasps

• No bonanza-type food • No fortress defense • Inheritance opportunities • Inbreeding limited • Allofeeding -> load lightening Helpers • Direct + indirect fitness

Non-wood-dwelling termites

Ants

• Ants (except species with gamergates) • Most bees • Non-wood-dwelling termites

Workers • Mainly indirect fitness

No bonanza-type food No fortress defense Few/no opportunities for inheritance Allofeeding -> load lightening

Type II • • • •

Shown are the characterizing traits, the evolved “Castes”, the driving evolutionary forces, the distribution of the three sociality types among taxa and likely evolutionary transitions between syndromes

Evolutionary transitions

Taxa

“Castes” Driving Factors

Characteristic traits

Table 12.2 Characterization of the three sociality syndromes

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Acknowledgements We thank all co-authors of the book for their contributions and helpful discussions of this last chapter. This synopsis greatly benefited from a fellowship at the Institute for Advanced Studies in Berlin (JK).

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Index

A actor 7 adoption 129, 185 aggregation 130, 194 aggression 97, 199, 212 alarm calls 247 Allee, W.C. 3 alliance 199, 229, 246 altruism 5, 37, 69, 153, 222, 246 ant tending 52 aphids. See also aphid soldiers 38, 62, 160, 162, 171, 245, 247 aphid soldiers density 50 development 49 ecological influences 47 evolution 40 genetic influences 45 life history 48 lifetime 51 morphology 42 phylogeny primary-host 40, 52 proximate influences 44 secondary-host 40, 52 Apis 111 Apoidea 107 assured Fitness Returns 20, 91 Atta 137

B Bathyergidae 206 bee 89, 108, 210, 247 benefit of philopatry hypothesis. See also hypothesis 163, 248 Bergmann’s rule 136 bioluminescence 17 bird 100, 163, 174, 247

bivoltinism 72 body size 112, 121, 166, 197 bonobos 230 budding 25, 130 bystander 200

C Cardiocondyla 135 caste 39, 51, 57, 127, 151, 154, 208, 253 Cerceris 109 chain rule 28 chimpanzee 199, 228 chromosomal translocations 153 cleaning 42 clonality 38, 247 clone clonal mixing 45, 48 cockroach 150 colony duration 50 fusion 131, 156, 159 growth 49 odor 132 colony size 49, 135, 152, 161, 214, 248 communal breeding. See also cooperative breeding 174 comparison sociality. See also sociality 121 competition 225 kin 22, 26 local mate 57 local resource 166, 247 scale of 27 competitors 26, 110, 157, 247 condition ecological 2, 108, 153, 214, 252 contextual analysis 12

261

262 cooperation 5, 13, 149, 174, 182, 199, 222, 245 cooperative breeders 173, 234 cooperative breeding. See also communal breeding 163, 174, 208, 245 cooperatively breeding vertebrates 100, 149, 163, 164 costs of helping 96, 164 costs of nest initiation 89 cross-fostering 183 Cryptocercidae 150 Cryptotermes secundus 153

D Darwin, C.R. 1, 2, 16 defens investment 37, 47 defenders. See also aphid soldiers 52 defense 42, 70, 97, 118, 120, 157, 227, 247, 248 despotism 232 digger wasps 107 direct fitness. See also fitness 1, 70, 92, 152, 163, 186, 213, 244, 247 direct fitness benefits 185 dispersal 17, 57, 160, 174, 195, 211, 215, 216, 228, 246, 247 disturbance 26 division of labor 17, 57, 76, 110, 161, 208 dominance 133, 198, 232

E eavesdropping 193, 200 ecological benefits of helping 89 ecological constraint 20, 63, 89, 164, 205, 246 ecological constraint hypothesis. See also hypothesis 163, 246 ecological parameters 127, 152 economic neighbourhood 27 efficiency foraging 113, 116, 121 elasticity 26 Emerson, A.E. 3 emigration 227 enforcement 14, 15 first order 15 second order 16 environmental constraints 129 environmentally-acquired recognition 181

Index Equidae 193 eusociality. See also Sociality 41, 58, 83, 110, 149, 205, 208, 216 Eustenogaster 99 evolutionary transitions 160, 253

F factory fortress 58 false workers 151 feeding competition 231 female philopatry 227 feralization 196 fertility 115 fig wasps 26 fire ants 18, 128 Fisher, R.A. 3, 4, 7 fission-fusion model 194 fitness direct 2, 6, 7, 8, 14, 15, 70, 92, 152, 163, 186, 213, 244, 247 inclusive 4, 7, 8, 63, 65, 128, 164, 176, 213, 244 indirect 2, 6, 7, 17, 49, 93, 157, 161, 176, 243, 253 maximisation 7, 8 neighbour-modulated 6, 7, 8, 9, 12, 27 food availability 155 foraging 90, 112, 137, 150, 156, 214, 226, 247 Formica 138 fortress defense 48, 247, 253 founding. See also nest founding 89, 107, 128 foundress 57, 107 functional monogyny 133 future fitness 96

G gall 37, 57 gall morphology 57 gall thrips 57 genetic relatedness. See also relatedness, kinship 1, 57, 128, 243 genetic structure 87, 225 gerontocracy 89 gorillas 228 greenbeard 18, 19, 244 group augmentation 101 group size. See also colony size 28, 87, 94, 96, 160, 197, 215, 231, 244

Index H habitat saturation 175 Hairy-Faced Hover Wasp 84 Haldane, J.B.S. 4, 22, 30, 32 Halictidae 111 Hamilton’s rule 8, 9, 19, 20, 21, 28, 64, 83, 128, 152, 176, 245 Hamilton, W.D. 4, 5, 6, 7, 8, 10, 13, 15, 17, 20, 21, 22, 28, 38, 46 haplodiploidy 38, 62, 65, 92, 108, 127, 152, 245, 247 haplodiploidy analogy 153 Hardin, G.J. 27 helper efficiency 114 value 113 helpers unrelated 179 helping 83 adjustment 178 effort 96 hibernation 130 hierarchy 136, 198 higher termites 152, 217, 247, 253 honey bees 16, 138 hopeful reproductives 156 host plant 39, 65, 136 hover wasps 83 abdominal substance 85 advantages for experimental work 90 colony genetic structure 89 distinguishing features 84 group size 85 nesting biology 85 relatedness 90 human 15, 16, 222 Huxley, J.S. 3 Hymenoptera 65, 83, 107, 127, 152, 243, 247, 253 hypothesis benefit of philopatry 163, 248 ecological constraint 163, 246 headstart 116 insurance 116 life history 163, 246 nest aggregation 119

I immigration 227 inbreeding 57, 89, 153, 196, 211, 216, 247, 250 inbreeding-outbreeding cycles 153 inbreeding avoidance 228, 247

263 incest avoidance 186, 214, 249 inclusive fitness. See also fitness 4, 7, 8, 63, 65, 128, 164, 176, 213, 244 indirect fitness. See also fitness 2, 6, 7, 17, 49, 93, 157, 161, 176, 243, 253 indirect recognition 179 Individual variation 96, 97 infanticide 3, 222 infanticide risk 228 inheritance 92, 100, 156, 162, 247, 248 inherited rank 198 instar extension 51 insurance. See also hypothesis 90 investment differential 117 parental 114, 116

K kin discrimination 17, 18, 173, 247 recognition 175, 186 selection. See also selection, Hamilton’s rule 8, 37, 152, 174, 218 222, 244 kinship. See also relatedness 8, 127, 152, 177, 221, 243, 245 kinship deceit hypothesis 185 Kladothrips 57 kleptoparasite 57 Koptothrips 58 Kropotkin, P.A. 2, 30

L Lasius 135 learned cues 184 leaving decisions 94, 211 lemurs 229 Leptothorax 130 life-history hypothesis. See also hypothesis 163 life history 48, 63, 109, 121, 151, 163, 181, 214, 246 life types 150 linkage 19 Liostenogaster 85 load-lightening 100, 247, 248 local mate competition. See also competition 57 local resource competition. See also competition 166, 247 long-tailed tit 182 longevity 66, 150, 161, 173, 215 lower termites 152

264 M male emigration 227 male fighting 62 male philopatry 228 mammals 165, 194, 205, 225, 246, 247, 253 manipulation 74, 155 market effects 225 mate guarding 63 mating 71 mating frequency 128, 134 mating system 71, 226 Maynard Smith, J. 8 Meliponinae 111 Microstigmus 110 migration 42, 227 Model Clades approach 59 Mole rats 67, 165, 205, 247 monogyny 131 morphological castes 152, 216 MP termites 150 multi-stallion bands 199 multilevel selection. See also selection 222, 244 multiple-pieces type termites 150 multiple mating 72, 134 Mutual Aid 2, 30 mutual benefit 5 mutualism 14, 16, 225, 247 Myrmica 140

N nepotism. See also kin discrimination 17, 232 nest defense 119, 120 nesting 85, 111, 130, 150 nesting sites 246 nest inheritance. See also inheritance 163, 248 nest repair 44 nests galls 47

O offspring dispersal 195 low quality 116 mortality 199 one-piece type termites 150 oP termites 150 outbreeding 65, 153, 216

Index P pair-living species 226 parasite 27, 107, 118, 119, 120, 121, 130, 197, 247 Trojan horse 118 parasite pressure 66, 132 parasitism 66, 107, 127, 247, 249 parasitoid 118 parasitoid wasps 18 parental care 60, 109, 174, 243, 247 parthenogenesis. See also clone 39 patrilines 227 partner choice 15, 16 Pheidole 137 Philanthus 113 philopatry 69, 163, 175, 209, 227, 248 female 227 male 227 phylogenetic constraints 226 phylogeny 37, 59, 151, 206 plasticity 111, 127 pleiotropy 14, 17, 18, 19 Pogonomyrmex 135 policing 16, 27, 46, 127 polyandry 134 polygyny 129 potential reproductive 121 predation 51, 157, 193, 194, 226, 247 predation risk 228 prey size 114 Price’s theorem 12 Price, G.R. 12 primates 221, 247 Prisoner’s Dilemma 15 provisioning 107, 117, 121, 164, 243 Przewalski’s horse 196 pseudergate 151 punishment 15, 16

Q queen number 127, 129 queens 216 queues 96

R reciprocity 15, 225 recognition. See also kin recognition templates 180 through learning 183 regressive molts 154

Index relatedness. See also kinship, genetic relatedness 5, 7, 8, 18, 19, 28, 38, 57, 156, 177, 212, 213, 221, 243, 245 asymmetry 62, 128 effective 26 repair 44 replacement reproductive 154 reproductive allocation 127 skew 20, 21, 57, 98, 127, 133, 211, 225 strategy 195 reputation 15 resource 62, 107, 111, 112, 113, 121 limitation 115 resource availability. See also food availability 159, 194 resource holding potential power 198 reversal. See also sociality loss 108 reward 15, 16 root nodules 16

S safe haven 160, 185, 251 selection fundamental theorem 4, 7 group 3, 11, 12, 14, 22, 26 hard 26 kin. See also kin selection 8 levels of 10, 11, 12, 13, 27 multilevel 222, 244 soft 12, 26 species 3, 14, 30 selfish herd 118, 193 selfishness 5, 225 semantics 5 sex allocation 71, 128 differences 227 ratio 57, 128, 138 Seychelles warbler 181 siderophore 17 sneak mating 199 social affiliation 194 social amoebae 18 sociality. See also eusociality 40 loss. See also reversal 40 sociality syndromes 250 social knowledge 201 organisation 226 parasitism 132 structure 226

265 society 225 socioecological model 231 soldier 39, 57, 154, 157, 248, 253 soldier aphids. See aphid soldiers 38 Solenopsis 133 solitary species 77, 210, 226 specialization 117 spite 5, 18, 27 split sex ratio 64, 138 stabilizing selection 158 Stenogastrinae 83 sterility 39 stress 197 stripe-backed wren 182 Sturtevant, A.H. 3 subfertility 95, 115 success reproductive 6, 94, 121 suicide evolutionary 29 supergene 18 survivorship insurance 91

T Temnothorax 131 termites 62, 100, 149, 215, 247, 253 territory 90, 174, 195 territory quality 175 thought experiment 18 thrips 40, 57, 160, 162, 247, 253 Thysanoptera 63 Tit For Tat 15 totipotent 1, 140, 151, 249 tragedy of the commons 27, 28, 29 tribe-splitting 26 true kin discrimination. See also kin discrimination 186, 247 true worker 162

V vampire bat 14, 28 venom 42 vertebrate social systems. See also cooperatively breeding vertebrates 100 virginity 64 virulence 27 viscosity 17, 22 vocalization 180

266 W wasp sphecid 108, 247 Wells, G.P. 3 Wells, H.G. 3 winged reproductives 154 wing loss 133 wing polymorphism 62

Index wing reduction 76 worker polymorphism 138 Wright, S. 4, 17, 22 Wynne-Edwards, V.C. 3

Z Zootermopsis nevadensis 159